Ionizing Radiation Stimulates Expression of Pro-Osteoclastogenic Genes in Marrow and Skeletal Tissue
Abstract
Exposure to ionizing radiation can cause rapid mineral loss and increase bone-resorbing osteoclasts within metabolically active, cancellous bone tissue leading to structural deficits. To better understand mechanisms involved in rapid, radiation-induced bone loss, we determined the influence of total body irradiation on expression of select cytokines known both to stimulate osteoclastogenesis and contribute to inflammatory bone disease. Adult (16 week), male C57BL/6J mice were exposed to either 2 Gy gamma rays (137Cs, 0.8 Gy/min) or heavy ions (56Fe, 600MeV, 0.50–1.1 Gy/min); this dose corresponds to either a single fraction of radiotherapy (typical total dose is ≥10 Gy) or accumulates over long-duration interplanetary missions. Serum, marrow, and mineralized tissue were harvested 4 h—7 days later. Gamma irradiation caused a prompt (2.6-fold within 4 h) and persistent (peaking at 4.1-fold within 1 day) rise in the expression of the obligate osteoclastogenic cytokine, receptor activator of nuclear factor kappa-B ligand (Rankl), within marrow cells over controls. Similarly, Rankl expression peaked in marrow cells within 3 days of iron exposure (9.2-fold). Changes in Rankl expression induced by gamma irradiation preceded and overlapped with a rise in expression of other pro-osteoclastic cytokines in marrow (eg, monocyte chemotactic protein-1 increased by 11.9-fold, and tumor necrosis factor-alphamore »
- Authors:
-
- NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States). Bone and Signaling Laboratory
- Publication Date:
- Research Org.:
- NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Space Biomedical Research Institute; National Aeronautics and Space Administration (NASA)
- OSTI Identifier:
- 1162232
- Alternate Identifier(s):
- OSTI ID: 1342731
- Report Number(s):
- 001
Journal ID: ISSN 1079-9907
- Grant/Contract Number:
- SC0001507; MA02501
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Interferon & Cytokine Research
- Additional Journal Information:
- Journal Volume: 35; Journal Issue: 6; Journal ID: ISSN 1079-9907
- Publisher:
- Mary Ann Liebert, Inc.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; bone; ionizing radiation; osteoclast; 63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT.
Citation Formats
Alwood, Joshua S., Shahnazari, Mohammad, Chicana, Betsabel, Schreurs, A. S., Kumar, Akhilesh, Bartolini, Alana, Shirazi-Fard, Yasaman, and Globus, Ruth K. Ionizing Radiation Stimulates Expression of Pro-Osteoclastogenic Genes in Marrow and Skeletal Tissue. United States: N. p., 2015.
Web. doi:10.1089/jir.2014.0152.
Alwood, Joshua S., Shahnazari, Mohammad, Chicana, Betsabel, Schreurs, A. S., Kumar, Akhilesh, Bartolini, Alana, Shirazi-Fard, Yasaman, & Globus, Ruth K. Ionizing Radiation Stimulates Expression of Pro-Osteoclastogenic Genes in Marrow and Skeletal Tissue. United States. https://doi.org/10.1089/jir.2014.0152
Alwood, Joshua S., Shahnazari, Mohammad, Chicana, Betsabel, Schreurs, A. S., Kumar, Akhilesh, Bartolini, Alana, Shirazi-Fard, Yasaman, and Globus, Ruth K. Thu .
"Ionizing Radiation Stimulates Expression of Pro-Osteoclastogenic Genes in Marrow and Skeletal Tissue". United States. https://doi.org/10.1089/jir.2014.0152. https://www.osti.gov/servlets/purl/1162232.
@article{osti_1162232,
title = {Ionizing Radiation Stimulates Expression of Pro-Osteoclastogenic Genes in Marrow and Skeletal Tissue},
author = {Alwood, Joshua S. and Shahnazari, Mohammad and Chicana, Betsabel and Schreurs, A. S. and Kumar, Akhilesh and Bartolini, Alana and Shirazi-Fard, Yasaman and Globus, Ruth K.},
abstractNote = {Exposure to ionizing radiation can cause rapid mineral loss and increase bone-resorbing osteoclasts within metabolically active, cancellous bone tissue leading to structural deficits. To better understand mechanisms involved in rapid, radiation-induced bone loss, we determined the influence of total body irradiation on expression of select cytokines known both to stimulate osteoclastogenesis and contribute to inflammatory bone disease. Adult (16 week), male C57BL/6J mice were exposed to either 2 Gy gamma rays (137Cs, 0.8 Gy/min) or heavy ions (56Fe, 600MeV, 0.50–1.1 Gy/min); this dose corresponds to either a single fraction of radiotherapy (typical total dose is ≥10 Gy) or accumulates over long-duration interplanetary missions. Serum, marrow, and mineralized tissue were harvested 4 h—7 days later. Gamma irradiation caused a prompt (2.6-fold within 4 h) and persistent (peaking at 4.1-fold within 1 day) rise in the expression of the obligate osteoclastogenic cytokine, receptor activator of nuclear factor kappa-B ligand (Rankl), within marrow cells over controls. Similarly, Rankl expression peaked in marrow cells within 3 days of iron exposure (9.2-fold). Changes in Rankl expression induced by gamma irradiation preceded and overlapped with a rise in expression of other pro-osteoclastic cytokines in marrow (eg, monocyte chemotactic protein-1 increased by 11.9-fold, and tumor necrosis factor-alpha increased by 1.7-fold over controls). The ratio, Rankl/Opg, in marrow increased by 1.8-fold, a net pro-resorption balance. In the marrow, expression of the antioxidant transcription factor, Nfe2l2, strongly correlated with expression levels of Nfatc1, Csf1, Tnf, and Rankl. Radiation exposure increased a serum marker of bone resorption (tartrate-resistant acid phosphatase) and led to cancellous bone loss (16% decrement after 1 week). Finally, we conclude that total body irradiation (gamma or heavy-ion) caused temporal elevations in the concentrations of specific genes expressed within marrow and mineralized tissue related to bone resorption, including select cytokines that lead to osteoclastogenesis and elevated resorption; this is likely to account for rapid and progressive deterioration of cancellous microarchitecture following exposure to ionizing radiation.},
doi = {10.1089/jir.2014.0152},
journal = {Journal of Interferon & Cytokine Research},
number = 6,
volume = 35,
place = {United States},
year = {Thu Jun 11 00:00:00 EDT 2015},
month = {Thu Jun 11 00:00:00 EDT 2015}
}
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Works referenced in this record:
Low-Dose, Ionizing Radiation and Age-Related Changes in Skeletal Microarchitecture
journal, January 2012
- Alwood, Joshua S.; Kumar, Akhilesh; Tran, Luan H.
- Journal of Aging Research, Vol. 2012
Heavy ion irradiation and unloading effects on mouse lumbar vertebral microarchitecture, mechanical properties and tissue stresses
journal, August 2010
- Alwood, J. S.; Yumoto, K.; Mojarrab, R.
- Bone, Vol. 47, Issue 2
Risk of Pelvic Fractures in Older Women Following Pelvic Irradiation
journal, November 2005
- Baxter, Nancy N.
- JAMA, Vol. 294, Issue 20
Guidelines for assessment of bone microstructure in rodents using micro-computed tomography
journal, June 2010
- Bouxsein, Mary L.; Boyd, Stephen K.; Christiansen, Blaine A.
- Journal of Bone and Mineral Research, Vol. 25, Issue 7
Functions of RANKL/RANK/OPG in bone modeling and remodeling
journal, May 2008
- Boyce, Brendan F.; Xing, Lianping
- Archives of Biochemistry and Biophysics, Vol. 473, Issue 2
Osteoclast differentiation and activation
journal, May 2003
- Boyle, William J.; Simonet, W. Scott; Lacey, David L.
- Nature, Vol. 423, Issue 6937
Pathways for Bone Loss in Inflammatory Disease
journal, April 2012
- Braun, Tobias; Schett, Georg
- Current Osteoporosis Reports, Vol. 10, Issue 2
Osteoclasts and CD8 T Cells Form a Negative Feedback Loop That Contributes to Homeostasis of Both the Skeletal and Immune Systems
journal, January 2013
- Buchwald, Zachary S.; Aurora, Rajeev
- Clinical and Developmental Immunology, Vol. 2013
Physiological Functions of Osteoblast Lineage and T Cell-Derived RANKL in Bone Homeostasis: CELLULAR SOURCES OF RANKL
journal, March 2014
- Fumoto, Toshio; Takeshita, Sunao; Ito, Masako
- Journal of Bone and Mineral Research, Vol. 29, Issue 4
A murine model for bone loss from therapeutic and space-relevant sources of radiation
journal, September 2006
- Hamilton, S. A.; Pecaut, M. J.; Gridley, D. S.
- Journal of Applied Physiology, Vol. 101, Issue 3
Vascular expression of the chemokine CX3CL1 promotes osteoclast recruitment and exacerbates bone resorption in an irradiated murine model
journal, April 2014
- Han, Ki Hoon; Ryu, Jae Won; Lim, Kyung-Eun
- Bone, Vol. 61
Mars' Surface Radiation Environment Measured with the Mars Science Laboratory's Curiosity Rover
journal, December 2013
- Hassler, D. M.; Zeitlin, C.; Wimmer-Schweingruber, R. F.
- Science, Vol. 343, Issue 6169
Nrf2 deficiency induces oxidative stress and promotes RANKL-induced osteoclast differentiation
journal, December 2013
- Hyeon, Seungha; Lee, Hyojung; Yang, Yoohee
- Free Radical Biology and Medicine, Vol. 65
Reduction in proximal femoral strength due to long-duration spaceflight
journal, March 2009
- Keyak, J. H.; Koyama, A. K.; LeBlanc, A.
- Bone, Vol. 44, Issue 3
Tumor Necrosis Factor α Stimulates Osteoclast Differentiation by a Mechanism Independent of the Odf/Rankl–Rank Interaction
journal, January 2000
- Kobayashi, Kanichiro; Takahashi, Naoyuki; Jimi, Eijiro
- Journal of Experimental Medicine, Vol. 191, Issue 2
Molecular Mechanisms Activating the Nrf2-Keap1 Pathway of Antioxidant Gene Regulation
journal, March 2005
- Kobayashi, Makoto; Yamamoto, Masayuki
- Antioxidants & Redox Signaling, Vol. 7, Issue 3-4
Oxidative stress and gamma radiation-induced cancellous bone loss with musculoskeletal disuse
journal, January 2010
- Kondo, Hisataka; Yumoto, Kenji; Alwood, Joshua S.
- Journal of Applied Physiology, Vol. 108, Issue 1
Osteoprotegerin A Physiological and Pharmacological Inhibitor of Bone Resorption.
journal, May 2001
- Kostenuik, Paul; Shalhoub, victoria
- Current Pharmaceutical Design, Vol. 7, Issue 8
Cortical and Trabecular Bone Mineral Loss From the Spine and Hip in Long-Duration Spaceflight
journal, March 2004
- Lang, Thomas; LeBlanc, Adrian; Evans, Harlan
- Journal of Bone and Mineral Research, Vol. 19, Issue 6
Adaptation of the Proximal Femur to Skeletal Reloading After Long-Duration Spaceflight
journal, May 2006
- Lang, Thomas F.; Leblanc, Adrian D.; Evans, Harlan J.
- Journal of Bone and Mineral Research, Vol. 21, Issue 8
Bone Marrow Stromal Cells Derived MCP-1 Reverses the Inhibitory Effects of Multiple Myeloma Cells on Osteoclastogenesis by Upregulating the RANK Expression
journal, December 2013
- Liu, Zhiqiang; Xu, Jingda; Li, Haiyan
- PLoS ONE, Vol. 8, Issue 12
Effect of proton irradiation followed by hindlimb unloading on bone in mature mice: A model of long-duration spaceflight
journal, October 2012
- Lloyd, Shane A.; Bandstra, Eric R.; Willey, Jeffrey S.
- Bone, Vol. 51, Issue 4
T cells: Critical bone regulators in health and disease
journal, September 2010
- Pacifici, Roberto
- Bone, Vol. 47, Issue 3
Role of T cells in ovariectomy induced bone loss-revisited
journal, January 2012
- Pacifici, Roberto
- Journal of Bone and Mineral Research, Vol. 27, Issue 2
Loss of Nrf2 accelerates ionizing radiation-induced bone loss by upregulating RANKL
journal, December 2012
- Rana, Tapasi; Schultz, Michelle A.; Freeman, Michael L.
- Free Radical Biology and Medicine, Vol. 53, Issue 12
Modulation of Osteoclast Differentiation and Function by the New Members of the Tumor Necrosis Factor Receptor and Ligand Families
journal, June 1999
- Suda, Tatsuo; Takahashi, Naoyuki; Udagawa, Nobuyuki
- Endocrine Reviews, Vol. 20, Issue 3
Absence of MCP-1 leads to elevated bone mass via impaired actin ring formation
journal, January 2012
- Sul, Ok-Joo; Ke, Ke; Kim, Woon-Ki
- Journal of Cellular Physiology, Vol. 227, Issue 4
Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems
journal, April 2007
- Takayanagi, Hiroshi
- Nature Reviews Immunology, Vol. 7, Issue 4
Acute exposure to high dose γ-radiation results in transient activation of bone lining cells
journal, November 2013
- Turner, Russell T.; Iwaniec, Urszula T.; Wong, Carmen P.
- Bone, Vol. 57, Issue 1
Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations
journal, January 2010
- Willey, Jeffrey S.; Livingston, Eric W.; Robbins, Michael E.
- Bone, Vol. 46, Issue 1
Ionizing Radiation and Bone Loss: Space Exploration and Clinical Therapy Applications
journal, March 2011
- Willey, Jeffrey S.; Lloyd, Shane A. J.; Nelson, Gregory A.
- Clinical Reviews in Bone and Mineral Metabolism, Vol. 9, Issue 1
Effect of radiation on the Notch signaling pathway in osteoblasts
journal, January 2013
- Yang, Bing; Tang, Quan; Post, Janine
- International Journal of Molecular Medicine, Vol. 31, Issue 3
Effect of radiation on the expression of osteoclast marker genes in RAW264.7 cells
journal, January 2012
- Yang, Bing; Zhou, Hui; Zhang, Xiao-Dong
- Molecular Medicine Reports, Vol. 5, Issue 4
CCR1 Chemokines Promote the Chemotactic Recruitment, RANKL Development, and Motility of Osteoclasts and Are Induced by Inflammatory Cytokines in Osteoblasts
journal, September 2004
- Yu, Xuefeng; Huang, Yuefang; Collin-Osdoby, Patricia
- Journal of Bone and Mineral Research, Vol. 19, Issue 12
Measurements of Energetic Particle Radiation in Transit to Mars on the Mars Science Laboratory
journal, May 2013
- Zeitlin, C.; Hassler, D. M.; Cucinotta, F. A.
- Science, Vol. 340, Issue 6136
Guidelines for assessment of bone microstructure in rodents using micro-computed tomography
journal, June 2010
- Bouxsein, Mary L.; Boyd, Stephen K.; Christiansen, Blaine A.
- Journal of Bone and Mineral Research, Vol. 25, Issue 7
Role of T cells in ovariectomy induced bone loss-revisited
journal, January 2012
- Pacifici, Roberto
- Journal of Bone and Mineral Research, Vol. 27, Issue 2
Pathways for Bone Loss in Inflammatory Disease
journal, April 2012
- Braun, Tobias; Schett, Georg
- Current Osteoporosis Reports, Vol. 10, Issue 2
Ionizing Radiation and Bone Loss: Space Exploration and Clinical Therapy Applications
journal, March 2011
- Willey, Jeffrey S.; Lloyd, Shane A. J.; Nelson, Gregory A.
- Clinical Reviews in Bone and Mineral Metabolism, Vol. 9, Issue 1
Functions of RANKL/RANK/OPG in bone modeling and remodeling
journal, May 2008
- Boyce, Brendan F.; Xing, Lianping
- Archives of Biochemistry and Biophysics, Vol. 473, Issue 2
Reduction in proximal femoral strength due to long-duration spaceflight
journal, March 2009
- Keyak, J. H.; Koyama, A. K.; LeBlanc, A.
- Bone, Vol. 44, Issue 3
Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations
journal, January 2010
- Willey, Jeffrey S.; Livingston, Eric W.; Robbins, Michael E.
- Bone, Vol. 46, Issue 1
Vascular expression of the chemokine CX3CL1 promotes osteoclast recruitment and exacerbates bone resorption in an irradiated murine model
journal, April 2014
- Han, Ki Hoon; Ryu, Jae Won; Lim, Kyung-Eun
- Bone, Vol. 61
Loss of Nrf2 accelerates ionizing radiation-induced bone loss by upregulating RANKL
journal, December 2012
- Rana, Tapasi; Schultz, Michelle A.; Freeman, Michael L.
- Free Radical Biology and Medicine, Vol. 53, Issue 12
Nrf2 deficiency induces oxidative stress and promotes RANKL-induced osteoclast differentiation
journal, December 2013
- Hyeon, Seungha; Lee, Hyojung; Yang, Yoohee
- Free Radical Biology and Medicine, Vol. 65
Solar particle events observed on MIR station
journal, June 1999
- Shurshakov, V. A.; Petrov, V. M.; Ivanov, YuV
- Radiation Measurements, Vol. 30, Issue 3
Osteoclast differentiation and activation
journal, May 2003
- Boyle, William J.; Simonet, W. Scott; Lacey, David L.
- Nature, Vol. 423, Issue 6937
Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems
journal, April 2007
- Takayanagi, Hiroshi
- Nature Reviews Immunology, Vol. 7, Issue 4
MCP-1 Is Induced by Receptor Activator of Nuclear Factor-κB Ligand, Promotes Human Osteoclast Fusion, and Rescues Granulocyte Macrophage Colony-stimulating Factor Suppression of Osteoclast Formation
journal, April 2005
- Kim, Michael S.; Day, Christopher J.; Morrison, Nigel A.
- Journal of Biological Chemistry, Vol. 280, Issue 16
MCP-1-induced Human Osteoclast-like Cells Are Tartrate-resistant Acid Phosphatase, NFATc1, and Calcitonin Receptor-positive but Require Receptor Activator of NFκB Ligand for Bone Resorption
journal, January 2006
- Kim, Michael S.; Day, Chris J.; Selinger, Christina I.
- Journal of Biological Chemistry, Vol. 281, Issue 2
Tumor Necrosis Factor α Stimulates Osteoclast Differentiation by a Mechanism Independent of the Odf/Rankl–Rank Interaction
journal, January 2000
- Kobayashi, Kanichiro; Takahashi, Naoyuki; Jimi, Eijiro
- Journal of Experimental Medicine, Vol. 191, Issue 2
Molecular Mechanisms Activating the Nrf2-Keap1 Pathway of Antioxidant Gene Regulation
journal, March 2005
- Kobayashi, Makoto; Yamamoto, Masayuki
- Antioxidants & Redox Signaling, Vol. 7, Issue 3-4
Physical basis of radiation protection in space travel
journal, November 2011
- Durante, Marco; Cucinotta, Francis A.
- Reviews of Modern Physics, Vol. 83, Issue 4
Measurements of Energetic Particle Radiation in Transit to Mars on the Mars Science Laboratory
journal, May 2013
- Zeitlin, C.; Hassler, D. M.; Cucinotta, F. A.
- Science, Vol. 340, Issue 6136
Mars' Surface Radiation Environment Measured with the Mars Science Laboratory's Curiosity Rover
journal, December 2013
- Hassler, D. M.; Zeitlin, C.; Wimmer-Schweingruber, R. F.
- Science, Vol. 343, Issue 6169
Oxidative stress and gamma radiation-induced cancellous bone loss with musculoskeletal disuse
journal, January 2010
- Kondo, Hisataka; Yumoto, Kenji; Alwood, Joshua S.
- Journal of Applied Physiology, Vol. 108, Issue 1
A murine model for bone loss from therapeutic and space-relevant sources of radiation
journal, September 2006
- Hamilton, S. A.; Pecaut, M. J.; Gridley, D. S.
- Journal of Applied Physiology, Vol. 101, Issue 3
Osteoclasts and CD8 T Cells Form a Negative Feedback Loop That Contributes to Homeostasis of Both the Skeletal and Immune Systems
journal, January 2013
- Buchwald, Zachary S.; Aurora, Rajeev
- Clinical and Developmental Immunology, Vol. 2013
Modulation of Osteoclast Differentiation and Function by the New Members of the Tumor Necrosis Factor Receptor and Ligand Families
journal, June 1999
- Suda, Tatsuo; Takahashi, Naoyuki; Udagawa, Nobuyuki
- Endocrine Reviews, Vol. 20, Issue 3
CCR1 Chemokines Promote the Chemotactic Recruitment, RANKL Development, and Motility of Osteoclasts and Are Induced by Inflammatory Cytokines in Osteoblasts
journal, September 2004
- Yu, Xuefeng; Huang, Yuefang; Collin-Osdoby, Patricia
- Journal of Bone and Mineral Research, Vol. 19, Issue 12
Bone Marrow Stromal Cells Derived MCP-1 Reverses the Inhibitory Effects of Multiple Myeloma Cells on Osteoclastogenesis by Upregulating the RANK Expression
journal, December 2013
- Liu, Zhiqiang; Xu, Jingda; Li, Haiyan
- PLoS ONE, Vol. 8, Issue 12
Interplanetary Crew Dose Rates for the August 1972 Solar Particle Event
journal, June 2000
- Parsons, Jennifer L.; Townsend, Lawrence W.
- Radiation Research, Vol. 153, Issue 6
Rapid Myeloid Recovery as a Possible Mechanism of Whole-Body Radioadaptive Response
journal, September 2008
- Otsuka, Kensuke; Koana, Takao; Tomita, Masanori
- Radiation Research, Vol. 170, Issue 3
Total-Body Irradiation of Postpubertal Mice with 137 Cs Acutely Compromises the Microarchitecture of Cancellous Bone and Increases Osteoclasts
journal, March 2009
- Kondo, Hisataka; Searby, Nancy D.; Mojarrab, Rose
- Radiation Research, Vol. 171, Issue 3
Short-Term Effects of Whole-Body Exposure to 56 Fe Ions in Combination with Musculoskeletal Disuse on Bone Cells
journal, April 2010
- Yumoto, Kenji; Globus, Ruth K.; Mojarrab, Rose
- Radiation Research, Vol. 173, Issue 4
Links between Innate Immunity and Normal Tissue Radiobiology
journal, April 2010
- Schaue, Dörthe; McBride, William H.
- Radiation Research, Vol. 173, Issue 4
Cytokines in Radiobiological Responses: A Review
journal, December 2012
- Schaue, Dörthe; Kachikwu, Evelyn L.; McBride, William H.
- Radiation Research, Vol. 178, Issue 6
Effect of proton irradiation followed by hindlimb unloading on bone in mature mice: A model of long-duration spaceflight
text, January 2012
- A., Bateman, Ted; Leidamarie, Tirado-Lee,; J., Pecaut, Michael
- The University of North Carolina at Chapel Hill University Libraries
Osteoprotegerin A Physiological and Pharmacological Inhibitor of Bone Resorption.
journal, May 2001
- Kostenuik, Paul; Shalhoub, victoria
- Current Pharmaceutical Design, Vol. 7, Issue 8
Effect of radiation on the Notch signaling pathway in osteoblasts
journal, January 2013
- Yang, Bing; Tang, Quan; Post, Janine
- International Journal of Molecular Medicine, Vol. 31, Issue 3
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journal, February 2016
- Schreurs, A. -S.; Shirazi-Fard, Y.; Shahnazari, M.
- Scientific Reports, Vol. 6, Issue 1
Differences in responses to X-ray exposure between osteoclast and osteoblast cells
journal, May 2017
- Zhang, Jian; Wang, Ziyang; Wu, Anqing
- Journal of Radiation Research, Vol. 58, Issue 6
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- Xiang, Lixin; Chen, Li; Xiang, Yang
- World Journal of Stem Cells
Maintenance of Near Normal Bone Mass and Architecture in Lethally Irradiated Female Mice following Adoptive Transfer with as few as 750 Purified Hematopoietic Stem Cells
journal, March 2019
- Deyhle, Richard T.; Wong, Carmen P.; Martin, Stephen A.
- Radiation Research, Vol. 191, Issue 5
Dose- and Ion-Dependent Effects in the Oxidative Stress Response to Space-Like Radiation Exposure in the Skeletal System
journal, October 2017
- Alwood, Joshua; Tran, Luan; Schreurs, Ann-Sofie
- International Journal of Molecular Sciences, Vol. 18, Issue 10
Oxidative Stress as Cause, Consequence, or Biomarker of Altered Female Reproduction and Development in the Space Environment
journal, November 2018
- Steller, Jon; Alberts, Jeffrey; Ronca, April
- International Journal of Molecular Sciences, Vol. 19, Issue 12