Exposure of the Bone Marrow Microenvironment to Simulated Solar and Galactic Cosmic Radiation Induces Biological Bystander Effects on Human Hematopoiesis

Almeida-Porada, Graca; Rodman, Christopher; Kuhlman, Bradford; Brudvik, Egil; Moon, John; George, Sunil; Guida, Peter; Sajuthi, Satria; Langefeld, Carl; Walker, Stephen; Wilson, Paul; Porada, Christopher

doi:10.1089/scd.2018.0005

Exposure of the Bone Marrow Microenvironment to Simulated Solar and Galactic Cosmic Radiation Induces Biological Bystander Effects on Human Hematopoiesis

Journal Article · Thu Apr 26 00:00:00 EDT 2018 · Stem Cells and Development

DOI:https://doi.org/10.1089/scd.2018.0005· OSTI ID:1430862

Almeida-Porada, Graca ^[1]; Rodman, Christopher ^[1]; Kuhlman, Bradford ^[1]; Brudvik, Egil ^[1]; Moon, John ^[1]; George, Sunil ^[1]; Guida, Peter ^[2]; Sajuthi, Satria ^[3]; Langefeld, Carl ^[3]; Walker, Stephen ^[1]; Wilson, Paul ^[4]; Porada, Christopher ^[1]

Wake Forest Univ., Winston-Salem, NC (United States). School of Medicine and Inst. for Regenerative Medicine
Brookhaven National Lab. (BNL), Upton, NY (United States). Biological, Environmental, and Climate Sciences Dept.
Wake Forest Univ., Winston-Salem, NC (United States). Center for Public Health Genomics and Dept. of Biostatistical Sciences and Division of Public Health Sciences
Univ. of California, Davis, CA (United States). Comprehensive Cancer Center and Dept. of Radiation Oncology

The stem cell compartment of the hematopoietic system constitutes one of the most radiosensitive tissues of the body and leukemias represent one of the most frequent radiogenic cancers with short latency periods. As such, leukemias may pose a particular threat to astronauts during prolonged space missions. Control of hematopoiesis is tightly governed by a specialized bone marrow (BM) microenvironment/niche. As such, any environmental insult that damages cells of this niche would be expected to produce pronounced effects on the types and functionality of hematopoietic/immune cells generated. We recently reported that direct exposure of human HSC to simulated SEP and GCR radiation dramatically altered the differentiative potential of these cells, and that simulated GCR exposures can directly induce DNA damage and mutations within human HSC, which led to leukemic transformation when these cells repopulated murine recipients. In the present study, we performed the first in depth examination to define changes that occur in mesenchymal stem cells (MSC) present in the human BM niche following exposure to accelerated protons and iron ions, and assess the impact these changes have upon human hematopoiesis. Here, our data thus provides compelling evidence that simulated SEP/GCR exposures can also contribute to defective hematopoiesis/immunity through so-called “biological bystander effects” by damaging the stromal cells that comprise the human marrow microenvironment, thereby altering their ability to support normal hematopoiesis.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0012704

OSTI ID:: 1430862

Report Number(s):: BNL--203398-2018-JAAM

Journal Information:: Stem Cells and Development, Journal Name: Stem Cells and Development Journal Issue: 18 Vol. 27; ISSN 1547-3287

Publisher:: Mary Ann Liebert, Inc.Copyright Statement

Country of Publication:: United States

Language:: English

References (80)

Efficient generation of human hepatocytes by the intrahepatic delivery of clonal human mesenchymal stem cells in fetal sheep Chamberlain, Jason; Yamagami, Takashi; Colletti, Evan Hepatology, Vol. 46, Issue 6 https://doi.org/10.1002/hep.21899	journal	December 2007
Differences amid bone marrow and cord blood hematopoietic stem/progenitor cell division kinetics da Silva, Cláudia Lobato; Gonçalves, Raquel; Porada, Christopher D. Journal of Cellular Physiology, Vol. 220, Issue 1 https://doi.org/10.1002/jcp.21736	journal	July 2009
Mesenchymal stem cells contribute to endogenous FVIII:c production Sanada, Chad; Kuo, Chung-Jung; Colletti, Evan J. Journal of Cellular Physiology, Vol. 228, Issue 5 https://doi.org/10.1002/jcp.24247	journal	January 2013
In vivo testing confirms a blunting of the human cell-mediated immune mechanism during space flight Taylor, Gerald R.; Janney, Robert P. Journal of Leukocyte Biology, Vol. 51, Issue 2 https://doi.org/10.1002/jlb.51.2.129	journal	February 1992
Effect of spaceflight on human stem cell hematopoiesis: suppression of erythropoiesis and myelopoiesis Davis, Thomas A.; Wiesmann, William; Kidwell, William Journal of Leukocyte Biology, Vol. 60, Issue 1 https://doi.org/10.1002/jlb.60.1.69	journal	July 1996
Mesenchymal stem cells Caplan, Arnold I. Journal of Orthopaedic Research, Vol. 9, Issue 5 https://doi.org/10.1002/jor.1100090504	journal	September 1991
Concise Review: The Surface Markers and Identity of Human Mesenchymal Stem Cells: Markers and Identity of MSCs Lv, Feng-Juan; Tuan, Rocky S.; Cheung, Kenneth M. C. STEM CELLS, Vol. 32, Issue 6 https://doi.org/10.1002/stem.1681	journal	May 2014
Establishing Criteria for Human Mesenchymal Stem Cell Potency: Establishing Criteria for hMSC Potency Samsonraj, Rebekah M.; Rai, Bina; Sathiyanathan, Padmapriya STEM CELLS, Vol. 33, Issue 6 https://doi.org/10.1002/stem.1982	journal	May 2015
Dynamic cell-cell interactions between cord blood haematopoietic progenitors and the cellular niche are essential for the expansion of CD34 ⁺ , CD34 ⁺ CD38 ⁻ and early lymphoid CD7 ⁺ cells da Silva, Cláudia Lobato; Gonçalves, Raquel; dos Santos, Francisco Journal of Tissue Engineering and Regenerative Medicine, Vol. 4, Issue 2 https://doi.org/10.1002/term.226	journal	February 2010
The Effect of Space and Parabolic Flight on Macrophage Hematopoiesis and Function Armstrong, Jason W.; Gerren, Richard A.; Chapes, Stephen K. Experimental Cell Research, Vol. 216, Issue 1 https://doi.org/10.1006/excr.1995.1020	journal	January 1995
Plasticity of Human Stem Cells in the Fetal Sheep Model of Human Stem Cell Transplantation Almeida-Porada, Graça; Porada, Christopher; Zanjani, Esmail D. International Journal of Hematology, Vol. 79, Issue 1 https://doi.org/10.1007/BF02983526	journal	January 2004
Split-dose exposures versus dual ion exposure in human cell neoplastic transformation Bennett, Paula V.; Cutter, Noelle C.; Sutherland, Betsy M. Radiation and Environmental Biophysics, Vol. 46, Issue 2 https://doi.org/10.1007/s00411-006-0091-y	journal	January 2007
Radiological health risks for exploratory class missions in space Nachtwey, D. Stuart; Yang, Tracy Chui-hsu Acta Astronautica, Vol. 23 https://doi.org/10.1016/0094-5765(91)90122-L	journal	January 1991
Effect of space flight on cytokine production Sonnenfeld, Gerald Acta Astronautica, Vol. 33 https://doi.org/10.1016/0094-5765(94)90119-8	journal	July 1994
Natural killer cells after altaïr mission Konstantinova, I. V.; Rykova, M.; Meshkov, D. Acta Astronautica, Vol. 36, Issue 8-12 https://doi.org/10.1016/0094-5765(95)00161-1	journal	October 1995
The natural cytotoxicity in cosmonauts on board space stations Meshkov, D.; Rykova, M. Acta Astronautica, Vol. 36, Issue 8-12 https://doi.org/10.1016/0094-5765(95)00162-X	journal	October 1995
Galactic cosmic rays and cell-hit frequencies outside the magnetosphere Curtis, S. B.; Letaw, J. R. Advances in Space Research, Vol. 9, Issue 10 https://doi.org/10.1016/0273-1177(89)90452-3	journal	January 1989
Radiation issues for piloted Mars mission Badhwar, Gautam D.; Stuart Nachtwey, D.; Chui-hsu Yang, Tracy Advances in Space Research, Vol. 12, Issue 2-3 https://doi.org/10.1016/0273-1177(92)90108-A	journal	January 1992
Simulated microgravity inhibits the genetic expression of interleukin-2 and its receptor in mitogen-activated T lymphocytes Walther, Isabelle; Pippia, Proto; Meloni, Maria Antonia FEBS Letters, Vol. 436, Issue 1 https://doi.org/10.1016/S0014-5793(98)01107-7	journal	September 1998
Radiation risk during long-term spaceflight Petrov, V. M. Advances in Space Research, Vol. 30, Issue 4 https://doi.org/10.1016/S0273-1177(02)00168-0	journal	January 2002
Effects of space flight and IGF-1 on immune function Chapes, S. K.; Simske, S. J.; Forsman, A. D. Advances in Space Research, Vol. 23, Issue 12 https://doi.org/10.1016/S0273-1177(99)00456-1	journal	January 1999
Mesenchymal stem cells Deans, Robert J.; Moseley, Annemarie B. Experimental Hematology, Vol. 28, Issue 8 https://doi.org/10.1016/S0301-472X(00)00482-3	journal	August 2000
Differentiative potential of human metanephric mesenchymal cells Almeida-Porada, G. Experimental Hematology, Vol. 30, Issue 12 https://doi.org/10.1016/S0301-472X(02)00967-0	journal	December 2002
Immune function during space flight Sonnenfeld, Gerald; Shearer, William T. Nutrition, Vol. 18, Issue 10 https://doi.org/10.1016/S0899-9007(02)00903-6	journal	October 2002
Mesenchymal stem cells as therapeutics and vehicles for gene and drug delivery Porada, Christopher D.; Almeida-Porada, Graça Advanced Drug Delivery Reviews, Vol. 62, Issue 12 https://doi.org/10.1016/j.addr.2010.08.010	journal	September 2010
Non-targeted effects induced by ionizing radiation: Mechanisms and potential impact on radiation induced health effects Morgan, William F.; Sowa, Marianne B. Cancer Letters, Vol. 356, Issue 1 https://doi.org/10.1016/j.canlet.2013.09.009	journal	January 2015
Mesenchymal stem cells derived from low risk acute lymphoblastic leukemia patients promote NK cell antitumor activity Entrena, Ana; Varas, Alberto; Vázquez, Miriam Cancer Letters, Vol. 363, Issue 2 https://doi.org/10.1016/j.canlet.2015.04.012	journal	July 2015
A human stromal-based serum-free culture system supports the ex vivo expansion/maintenance of bone marrow and cord blood hematopoietic stem/progenitor cells da Silva, Cláudia Lobato; Gonçalves, Raquel; Crapnell, Kirsten B. Experimental Hematology, Vol. 33, Issue 7 https://doi.org/10.1016/j.exphem.2005.03.017	journal	July 2005
A Stro-1+ human universal stromal feeder layer to expand/maintain human bone marrow hematopoietic stem/progenitor cells in a serum-free culture system Gonçalves, Raquel; Lobato da Silva, Cláudia; Cabral, Joaquim M. S. Experimental Hematology, Vol. 34, Issue 10 https://doi.org/10.1016/j.exphem.2006.05.024	journal	October 2006
The evolving view of the hematopoietic stem cell niche Beerman, Isabel; Luis, Tiago C.; Singbrant, Sofie Experimental Hematology, Vol. 50 https://doi.org/10.1016/j.exphem.2017.01.008	journal	June 2017
The bone marrow microenvironment is a critical player in the NK cell response against acute myeloid leukaemia in vitro Vasold, Jochen; Wagner, Michaela; Drolle, Heidrun Leukemia Research, Vol. 39, Issue 2 https://doi.org/10.1016/j.leukres.2014.12.001	journal	February 2015
Human blood and marrow side population stem cell and Stro-1 positive bone marrow stromal cell numbers decline with age, with an increase in quality of surviving stem cells: Correlation with cytokines Brusnahan, S. K.; McGuire, T. R.; Jackson, J. D. Mechanisms of Ageing and Development, Vol. 131, Issue 11-12 https://doi.org/10.1016/j.mad.2010.10.002	journal	November 2010
Non-targeted effects of ionising radiation—Implications for low dose risk Kadhim, Munira; Salomaa, Sisko; Wright, Eric Mutation Research/Reviews in Mutation Research, Vol. 752, Issue 2 https://doi.org/10.1016/j.mrrev.2012.12.001	journal	April 2013
Pericytes, integral components of adult hematopoietic stem cell niches Sá da Bandeira, D.; Casamitjana, J.; Crisan, M. Pharmacology & Therapeutics, Vol. 171 https://doi.org/10.1016/j.pharmthera.2016.11.006	journal	March 2017
Generation of tissue-specific cells from MSC does not require fusion or donor-to-host mitochondrial/membrane transfer Colletti, Evan J.; Airey, Judith A.; Liu, Wansheng Stem Cell Research, Vol. 2, Issue 2 https://doi.org/10.1016/j.scr.2008.08.002	journal	March 2009
Regulation of Hematopoietic Stem Cells by the Niche Arai, Fumio; Hirao, Atsushi; Suda, Toshio Trends in Cardiovascular Medicine, Vol. 15, Issue 2 https://doi.org/10.1016/j.tcm.2005.03.002	journal	February 2005
Human Wharton's jelly mesenchymal stem cell secretome display antiproliferative effect on leukemia cell line and produce additive cytotoxic effect in combination with doxorubicin Hendijani, Fatemeh; Haghjooy Javanmard, Shaghayegh; Sadeghi-aliabadi, Hojjat Tissue and Cell, Vol. 47, Issue 3 https://doi.org/10.1016/j.tice.2015.01.005	journal	June 2015
In vitro and in vivo assessment of direct effects of simulated solar and galactic cosmic radiation on human hematopoietic stem/progenitor cells Rodman, C.; Almeida-Porada, G.; George, S. K. Leukemia, Vol. 31, Issue 6 https://doi.org/10.1038/leu.2016.344	journal	November 2016
Defining the transcriptome and proteome in three functionally different human cell lines Lundberg, Emma; Fagerberg, Linn; Klevebring, Daniel Molecular Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1038/msb.2010.106	journal	January 2010
Sequence signatures and mRNA concentration can explain two‐thirds of protein abundance variation in a human cell line Vogel, Christine; de Sousa Abreu, Raquel; Ko, Daijin Molecular Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1038/msb.2010.59	journal	January 2010
Osteoblastic cells regulate the haematopoietic stem cell niche Calvi, L. M.; Adams, G. B.; Weibrecht, K. W. Nature, Vol. 425, Issue 6960 https://doi.org/10.1038/nature02040	journal	October 2003
Identification of the haematopoietic stem cell niche and control of the niche size Zhang, Jiwang; Niu, Chao; Ye, Ling Nature, Vol. 425, Issue 6960 https://doi.org/10.1038/nature02041	journal	October 2003
Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor Adams, Gregor B.; Chabner, Karissa T.; Alley, Ian R. Nature, Vol. 439, Issue 7076 https://doi.org/10.1038/nature04247	journal	December 2005
Global quantification of mammalian gene expression control Schwanhäusser, Björn; Busse, Dorothea; Li, Na Nature, Vol. 473, Issue 7347 https://doi.org/10.1038/nature10098	journal	May 2011
Heavy ion carcinogenesis and human space exploration Durante, Marco; Cucinotta, Francis A. Nature Reviews Cancer, Vol. 8, Issue 6, p. 465-472 https://doi.org/10.1038/nrc2391	journal	May 2008
Adult haematopoietic stem cell niches Crane, Genevieve M.; Jeffery, Elise; Morrison, Sean J. Nature Reviews Immunology, Vol. 17, Issue 9 https://doi.org/10.1038/nri.2017.53	journal	June 2017
Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth Ramasamy, R.; Lam, E. W-F; Soeiro, I. Leukemia, Vol. 21, Issue 2 https://doi.org/10.1038/sj.leu.2404489	journal	December 2006
Radiation-induced genomic instability and bystander effects: inter-related nontargeted effects of exposure to ionizing radiation Lorimore, Sally A.; Coates, Philip J.; Wright, Eric G. Oncogene, Vol. 22, Issue 45 https://doi.org/10.1038/sj.onc.1207044	journal	October 2003
Adult Stem Cell Plasticity and Methods of Detection Almeida-Porada, Graca; Porada, Christopher; Zanjani, Esmail D. Reviews in Clinical and Experimental Hematology, Vol. 5, Issue 1 https://doi.org/10.1046/j.1468-0734.2001.00027.x	journal	March 2001
Microenvironment and stem properties of bone marrow-derived mesenchymal cells Bianchi, Giordano; Muraglia, Anita; Daga, Antonio Wound Repair and Regeneration, Vol. 9, Issue 6 https://doi.org/10.1046/j.1524-475x.2001.00460.x	journal	November 2001
Immune Responses in Space Flight Sonnenfeld, G. International Journal of Sports Medicine, Vol. 19, Issue S 3 https://doi.org/10.1055/s-2007-971992	journal	July 1998
Integrated Genomic and Proteomic Analyses of Gene Expression in Mammalian Cells Tian, Qiang; Stepaniants, Serguei B.; Mao, Mao Molecular & Cellular Proteomics, Vol. 3, Issue 10 https://doi.org/10.1074/mcp.M400055-MCP200	journal	October 2004
Radiation-induced genomic instability and bystander effects: related inflammatory-type responses to radiation-induced stress and injury? A review Lorimore, S. A.; Wright, E. G. International Journal of Radiation Biology, Vol. 79, Issue 1 https://doi.org/10.1080/0955300021000045664	journal	January 2003
Marrow Stem Cells, Mesenchymal Progenitor Cells, and Stromal Progeny La Russa, Vincent F.; Schwarzenberger, Paul; Miller, Alan Cancer Investigation, Vol. 20, Issue 1 https://doi.org/10.1081/CNV-120000372	journal	January 2002
Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size Stier, Sebastian; Ko, Yon; Forkert, Randolf Journal of Experimental Medicine, Vol. 201, Issue 11 https://doi.org/10.1084/jem.20041992	journal	May 2005
Altered Cytokine Production by Specific Human Peripheral Blood Cell Subsets Immediately Following Space Flight Crucian, Brian E.; Cubbage, Michael L.; Sams, Clarence F. Journal of Interferon & Cytokine Research, Vol. 20, Issue 6 https://doi.org/10.1089/10799900050044741	journal	June 2000
Implications of the space radiation environment for human exploration in deep space Townsend, Lawrence W. Radiation Protection Dosimetry, Vol. 115, Issue 1-4 https://doi.org/10.1093/rpd/nci141	journal	December 2005
Loss of T cell precursors after spaceflight and exposure to vector‐averaged gravity Woods, Chris C.; Banks, Krista E.; Gruener, Raphael The FASEB Journal, Vol. 17, Issue 11 https://doi.org/10.1096/fj.02-0749fje	journal	June 2003
Role of mesenchymal stem cells in hematopoietic stem cell transplantation Devine, Steven M.; Hoffman, Ron Current Opinion in Hematology, Vol. 7, Issue 6 https://doi.org/10.1097/00062752-200011000-00007	journal	January 2000
Modeling the Acute Health Effects of Astronauts from Exposure to Large Solar Particle Events Hu, Shaowen; Kim, Myung-Hee Y.; McClellan, Gene E. Health Physics, Vol. 96, Issue 4 https://doi.org/10.1097/01.HP.0000339020.92837.61	journal	January 2009
Physical basis of radiation protection in space travel Durante, Marco; Cucinotta, Francis A. Reviews of Modern Physics, Vol. 83, Issue 4 https://doi.org/10.1103/RevModPhys.83.1245	journal	November 2011
Perivascular Stromal Cells as a Potential Reservoir of Human Cytomegalovirus: HCMV Infects Perivascular Stromal Cells Soland, M. A.; Keyes, L. R.; Bayne, R. American Journal of Transplantation, Vol. 14, Issue 4 https://doi.org/10.1111/ajt.12642	journal	March 2014
Development of a novel assay to evaluate the functional potential of umbilical cord blood progenitors Reems, Jo-Anna; Hall, Karen M.; Gebru, Luladay H. Transfusion, Vol. 48, Issue 4 https://doi.org/10.1111/j.1537-2995.2007.01586.x	journal	April 2008
Selected Stro-1-enriched bone marrow stromal cells display a major suppressive effect on lymphocyte proliferation: STRO1+ MSC SUBSET INHIBITS LYMPHOCYTE PROLIFERATION Nasef, A.; Zhang, Y. Z.; Mazurier, C. International Journal of Laboratory Hematology, Vol. 31, Issue 1 https://doi.org/10.1111/j.1751-553X.2007.00997.x	journal	January 2009
Cell sensitivity to gravity Cogoli, A.; Tschopp, A.; Fuchs-Bislin, P. Science, Vol. 225, Issue 4658 https://doi.org/10.1126/science.6729481	journal	July 1984
Effect of spaceflight on natural killer cell activity Rykova, M. P.; Sonnenfeld, G.; Lesnyak, A. T. Journal of Applied Physiology, Vol. 73, Issue 2 https://doi.org/10.1152/jappl.1992.73.2.S196	journal	August 1992
Human Mesenchymal Stem Cells Form Purkinje Fibers in Fetal Sheep Heart Airey, Judith A.; Almeida-Porada, Graça; Colletti, Evan J. Circulation, Vol. 109, Issue 11 https://doi.org/10.1161/01.CIR.0000124222.16321.26	journal	March 2004
Mesenchymal Stem Cells Minguell, José J.; Erices, Alejandro; Conget, Paulette Experimental Biology and Medicine, Vol. 226, Issue 6 https://doi.org/10.1177/153537020122600603	journal	June 2001
Formation of human hepatocytes by human hematopoietic stem cells in sheep Almeida-Porada, Graça; Porada, Christopher D.; Chamberlain, Jason Blood, Vol. 104, Issue 8 https://doi.org/10.1182/blood-2004-01-0259	journal	October 2004
Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche Taichman, Russell S. Blood, Vol. 105, Issue 7 https://doi.org/10.1182/blood-2004-06-2480	journal	April 2005
The radiation-induced bystander effect: evidence and significance Azzam, Edouard I.; Little, John B. Human & Experimental Toxicology, Vol. 23, Issue 2 https://doi.org/10.1191/0960327104ht418oa	journal	February 2004
Human Bone Marrow Mesenchymal Stem Cells Display Anti-Cancer Activity in SCID Mice Bearing Disseminated Non-Hodgkin's Lymphoma Xenografts Secchiero, Paola; Zorzet, Sonia; Tripodo, Claudio PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011140	journal	June 2010
Assessing Exposure to Cosmic Radiation during Long-haul Flights Bottollier-Depois, Jean-François; Chau, Quang; Bouisset, Patrick Radiation Research, Vol. 153, Issue 5 https://doi.org/10.1667/0033-7587(2000)153[0526:AETCRD]2.0.CO;2	journal	May 2000
Interplanetary Crew Dose Rates for the August 1972 Solar Particle Event Parsons, Jennifer L.; Townsend, Lawrence W. Radiation Research, Vol. 153, Issue 6 https://doi.org/10.1667/0033-7587(2000)153[0729:ICDRFT]2.0.CO;2	journal	June 2000
Space Radiation Cancer Risks and Uncertainties for Mars Missions Cucinotta, Francis A.; Schimmerling, Walter; Wilson, John W. Radiation Research, Vol. 156, Issue 5 https://doi.org/10.1667/0033-7587(2001)156[0682:SRCRAU]2.0.CO;2	journal	November 2001
Shuttle Radiation Dose Measurements in the International Space Station Orbits ¹ Badhwar, Gautam D. Radiation Research, Vol. 157, Issue 1 https://doi.org/10.1667/0033-7587(2002)157[0069:SRDMIT]2.0.CO;2	journal	January 2002
Proton-HZE-Particle Sequential Dual-Beam Exposures Increase Anchorage-Independent Growth Frequencies in Primary Human Fibroblasts Zhou, Guangming; Bennett, Paula V.; Cutter, Noelle C. Radiation Research, Vol. 166, Issue 3 https://doi.org/10.1667/RR0596.1	journal	September 2006
Threshold-Type Dose Response for Induction of Neoplastic Transformation by 1 GeV/nucleon Iron Ions Elmore, E.; Lao, X-Y.; Kapadia, R. Radiation Research, Vol. 171, Issue 6 https://doi.org/10.1667/RR1673.1	journal	June 2009
Neoplastic Transformation In Vitro by Mixed Beams of High-Energy Iron Ions and Protons Elmore, E.; Lao, X-Y.; Kapadia, R. Radiation Research, Vol. 176, Issue 3 https://doi.org/10.1667/RR2646.1	journal	September 2011
The Effects of Delta Rays on the Number of Particle-Track Traversals per Cell in Laboratory and Space Exposures Cucinotta, Francis A.; Nikjoo, Hooshang; Goodhead, Dudley T. Radiation Research, Vol. 150, Issue 1 https://doi.org/10.2307/3579651	journal	July 1998

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Exposure of the Bone Marrow Microenvironment to Simulated Solar and Galactic Cosmic Radiation Induces Biological Bystander Effects on Human Hematopoiesis

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