Whole-body proton irradiation causes long-term damage to hematopoietic stem cells in mice

Radiation Research

Volumn 183, Issue 2, 2015, Pages 240-248

  Chang, Jianhui ^a   Feng, Wei ^a   Wang, Yingying ^a   Luo, Yi ^a   Allen, Antiño R ^a   Koturbash, Igor ^a   Turner, Jennifer ^b   Stewart, Blair ^b   Raber, Jacob ^b,c   Hauer Jensen, Martin ^a   Zhou, Daohong ^a   Shao, Lijian ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; PROTON;

ANIMAL EXPERIMENT; ARTICLE; BLOOD; BLOOD CELL; BONE MARROW; BURST FORMING UNIT E; CELL COUNT; CELL DAMAGE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CLONOGENESIS; COLONY FORMING CELL; COLONY FORMING UNIT GEMM; COLONY FORMING UNIT GM; CONTROLLED STUDY; DNA DAMAGE; ERYTHROCYTE; FLOW CYTOMETRY; GRANULOCYTE; HEMATOPOIETIC STEM CELL; INFANT; MALE; MEGAKARYOCYTE; MONOCYTE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTON RADIATION; RADIATION DOSE; RADIATION EXPOSURE; RADIATION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHOLE BODY PROTON IRRADIATION; WHOLE BODY RADIATION; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CELL CULTURE; COSMIC RADIATION; LONGITUDINAL STUDY; METABOLISM; PATHOLOGY; PHYSIOLOGY; RADIATION RESPONSE;

MUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; COSMIC RADIATION; DOSE-RESPONSE RELATIONSHIP, RADIATION; HEMATOPOIETIC STEM CELLS; LONGITUDINAL STUDIES; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PROTONS; RADIATION DOSAGE; REACTIVE OXYGEN SPECIES; WHOLE-BODY IRRADIATION;

EID: 84923315652     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR13887.1     Document Type: Article

References (42)

1. Moore FD. Radiation burdens for humans on prolonged exomagnetospheric voyages. FASEB J 1992; 6:2338-43.
2. Townsend LW. Implications of the space radiation environment for human exploration in deep space. Radiat Prot Dosimetry 2005; 115:44-50.
3. Cengel KA, Diffenderfer ES, Avery S, Kennedy AR, McDonough J. Using electron beam radiation to simulate the dose distribution for whole body solar particle event proton exposure. Radiat Environ Biophys 2010; 49:715-21.
4. Simonsen LC, Cucinotta FA, Atwell W, Nealy JE. Temporal analysis of the October 1989 proton flare using computerized anatomical models. Radiat Res 1993; 133:1-11.
5. Parsons JL, Townsend LW. Interplanetary crew dose rates for the August 1972 solar particle event. Radiat Res 2000; 153:729-33.
6. Raju MR. Proton radiobiology, radiosurgery and radiotherapy. Int J Radiat Biol 1995; 67:237-59.
7. Loeffler JS, Smith AR, Suit HD. The potential role of proton beams in radiation oncology. Semin Oncol 1997; 24:686-95.
8. Shao L, Luo Y, Zhou D. Hematopoietic stem cell injury induced by ionizing radiation. Antioxid Redox Signal 2014; 20:1447-62.
9. Shao L, Wang Y, Chang J, Luo Y, Meng A, Zhou D. Hematopoietic stem cell senescence and cancer therapy-induced long-Term bone marrow injury. Transl Cancer Res 2013; 2:397-411.
10. Harrington NP, Chambers KA, Ross WM, Filion LG. Radiation damage and immune suppression in splenic mononuclear cell populations. Clin Exp Immunol 1997; 107:417-24.
11. Chambers KA, Harrington NP, Ross WM, Filion LG. Relative alterations in blood mononuclear cell populations reflect radiation injury in mice. Cytometry 1998; 31:45-52.
12. Kajioka EH, Andres ML, Li J, Mao XW, Moyers MF, Nelson GA, et al. Acute effects of whole-body proton irradiation on the immune system of the mouse. Radiat Res 2000; 153:587-94.
13. Gridley DS, Rizvi A, Luo-Owen X, Makinde AY, Coutrakon GB, Koss P, et al. Variable hematopoietic responses to acute photons, protons and simulated solar particle event protons. In Vivo 2008; 22:159-69.
14. Ware JH, Sanzari J, Avery S, Sayers C, Krigsfeld G, Nuth M, et al. Effects of proton radiation dose, dose rate and dose fractionation on hematopoietic cells in mice. Radiat Res 2010; 174:325-30.
15. Maks CJ, Wan XS, Ware JH, Romero-Weaver AL, Sanzari JK, Wilson JM, et al. Analysis of white blood cell counts in mice after gamma- or proton-radiation exposure. Radiat Res 2011; 176:170-6.
16. Luo-Owen X, Pecaut MJ, Rizvi A, Gridley DS. Low-dose totalbody gamma irradiation modulates immune response to acute proton radiation. Radiat Res 2012; 177:251-64.
17. Sanzari JK, Cengel KA, Steven Wan X, Rusek A, Kennedy AR. Acute hematological effects in mice exposed to the expected doses, dose-rates, and energies of solar particle event-like proton radiation. Life Sci Space Res 2014; 2:86-91.
18. Wagemaker G. Heterogeneity of radiation sensitivity of hemopoietic stem cell subsets. Stem Cells 1995; 13 Suppl 1:257-60.
19. Gridley DS, Pecaut MJ. Whole-body irradiation and long-Term modification of bone marrow-derived cell populations by low- And high-LET radiation. In Vivo 2006; 20:781-9.
20. Wang Y, Schulte BA, LaRue AC, Ogawa M, Zhou D. Total body irradiation selectively induces murine hematopoietic stem cell senescence. Blood 2006; 107:358-66.
21. Li H, Wang Y, Pazhanisamy SK, Shao L, Batinic-Haberle I, Meng A, et al. Mn(III) meso-Tetrakis-(N-ethylpyridinium-2-yl) porphyrin mitigates total body irradiation-induced long-Term bone marrow suppression. Free Radic Biol Med 2011; 51:30-7.
22. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128:325-39.
23. Shao L, Feng W, Li H, Gardner D, Luo Y, Wang Y, et al. Total body irradiation causes long-Term mouse BM injury via induction of HSC premature senescence in an Ink4a- And Arf-independent manner. Blood 2014; 123:3105-15.
24. Ploemacher RE, van der Sluijs JP, Voerman JS, Brons NH. An in vitro limiting-dilution assay of long-Term repopulating hematopoietic stem cells in the mouse. Blood 1989; 74:2755-63.
25. Wang Y, Liu L, Pazhanisamy SK, Li H, Meng A, Zhou D. Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic Biol Med 2010; 48:348-56.
26. Norbury CJ, Hickson ID. Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 2001; 41:367-401.
27. Major IR, Mole RH. Myeloid leukaemia in x-ray irradiated CBA mice. Nature 1978; 272:455-6.
28. Shimizu Y, Kato H, Schull WJ. Risk of cancer among atomic bomb survivors. J Radiat Res 1991; 32 Suppl 2:54-63.
29. Kennedy AR, Davis JG, Carlton W, Ware JH. Effects of dietary antioxidant supplementation on the development of malignant lymphoma and other neoplastic lesions in mice exposed to proton or iron-ion radiation. Radiat Res 2008; 169:615-25.
30. Sanzari JK, Wan SX, Diffenderfer ES, Cengel KA, Kennedy AR. Relative biological effectiveness of simulated solar particle event proton radiation to induce acute hematological change in the porcine model. J Radiat Res 2014; 55:228-44.
31. Desai N, Davis E, O'Neill P, Durante M, Cucinotta FA, Wu H. Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation. Radiat Res 2005; 164:518-22.
32. Goetz W, Morgan MN, Baulch JE. The effect of radiation quality on genomic DNA methylation profiles in irradiated human cell lines. Radiat Res 2011; 175:575-87.
33. Tian J, Zhao W, Tian S, Slater JM, Deng Z, Gridley DS. Expression of genes involved in mouse lung cell differentiation/ regulation after acute exposure to photons and protons with or without low-dose preirradiation. Radiat Res 2011; 176:553-64.
34. Di Pietro C, Piro S, Tabbi G, Ragusa M, Di Pietro V, Zimmitti V, et al. Cellular and molecular effects of protons: apoptosis induction and potential implications for cancer therapy. Apoptosis 2006; 11:57-66.
35. Pazhanisamy SK, Li H, Wang Y, Batinic-Haberle I, Zhou D. NADPH oxidase inhibition attenuates total body irradiationinduced haematopoietic genomic instability. Mutagenesis 2011; 26:431-5.
36. Giedzinski E, Rola R, Fike JR, Limoli CL. Efficient production of reactive oxygen species in neural precursor cells after exposure to 250 MeV protons. Radiat Res 2005; 164:540-4.
37. Baluchamy S, Ravichandran P, Periyakaruppan A, Ramesh V, Hall JC, Zhang Y, et al. Induction of cell death through alteration of oxidants and antioxidants in lung epithelial cells exposed to high energy protons. J Biol Chem 2010; 285:24769-74.
38. Wambi CO, Sanzari JK, Sayers CM, Nuth M, Zhou Z, Davis J, et al. Protective effects of dietary antioxidants on proton total-body irradiation-mediated hematopoietic cell and animal survival. Radiat Res 2009; 172:175-86.
39. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, et al. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010; 7:391-402.
40. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008; 135:1118-29.
41. Chen C, Liu Y, Liu R, Ikenoue T, Guan KL, Liu Y, et al. TSCmTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 2008; 205:2397-408.
42. Schuringa JJ, Vellenga E. Role of the polycomb group gene BMI1 in normal and leukemic hematopoietic stem and progenitor cells. Curr Opin Hematol 2010; 17:294-9.