Stem cell niches and other factors that influence the sensitivity of bone marrow to radiation-induced bone cancer and leukaemia in children and adults

International Journal of Radiation Biology

Volumn 87, Issue 4, 2011, Pages 343-359

  Richardson, Richard B ^a  

^a ATOMIC ENERGY OF CANADA LIMITED   (Canada)

Author keywords

bone; cancer predisposition; radiation induced tumours; stem cells

Indexed keywords

OXYGEN;

ADULT; AGE; ARTICLE; BONE CANCER; BONE MARROW; CANCER INCIDENCE; CHILD; CHONDROSARCOMA; EWING SARCOMA; FIBROSARCOMA; FIBROSIS; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMIA; NONHUMAN; OSTEOBLAST; OSTEOSARCOMA; PAGET BONE DISEASE; PRIORITY JOURNAL; RADIATION; RADIOSENSITIVITY; RISK FACTOR; STEM CELL; STEM CELL NICHE;

ADULT; BONE MARROW; BONE NEOPLASMS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; LEUKEMIA; MALE; NEOPLASMS, RADIATION-INDUCED; RADIATION TOLERANCE; STEM CELLS;

EID: 79953790905     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.3109/09553002.2010.537430     Document Type: Article

References (123)

1. Albagha OM, Visconti MR, Alonso N, Langston AL, Cundy T, Dargie R, Dunlop MG, Fraser WD, Hooper MJ, Isaia G, Nicholson GC, del Pino Montes J, Gonzalez-Sarmiento R, di Stefano M, Tenesa A, Walsh JP, Ralston SH. 2010. Genomewide association study identifies variants at CSF1, OPTN and TNFRSF11A as genetic risk factors for Paget's disease of bone. Nature Genetics 42:520-524.
2. Arai F, Suda T. 2007. Maintenance of quiescent hematopoietic stem cells in the osteoblastic niche. Annals of the New York Academy of Sciences 1106:41-53. (Pubitemid 47443041)
3. Committee on the Biological Effects of Ionizing Radiation BEIR IV 1988 Health effects of radon and other internally deposited alpha-emitters. Committee on the Biological Effects of Ionizing Radiation National Research Council. Washington DC: National Academy Press.
4. Committee on the Biological Effects of Ionizing Radiation BEIR V 1990 Health effects of exposure to low levels of ionizing radiation. Committee on the Biological Effects of Ionizing Radiation, National Research Council. Washington DC: National Academy Press.
5. Committee on the Biological Effects of Ionizing Radiation (BEIR VII). 2006. Health risks from exposure to low levels of ionizing radiation, Phase 2. Committee on the Biological Effects of Ionizing Radiation, National Research Council. Washington DC: National Academy Press.
6. Bianco P, Riminucci M, Gronthos S, Robey PG. 2001. Bone marrow stromal stem cells: Nature, biology, and potential applications. Stem Cells 19:180-192. (Pubitemid 32524539)
7. Bithell JF, Stewart AM. 1975. Prenatal irradiation and childhood malignancy: A review of British data from the Oxford survey. British Journal of Cancer 31:271-307.
8. Boice JD Jr, Blettner M, Kleinerman RA, Stovall M, Moloney WC, Engholm G, Austin DF, Bosch A, Cookfair DL, Krementz ET, Latourette HB, Peters LJ, Schulz MD, Lundell M, Pettersson F, Storm HH, Bell CMJ, Coleman MP, Fraser P, Palmer M. 1987. Radiation dose and leukemia risk in patients treated for cancer of the cervix. Journal of the National Cancer Institute 79:1295-1311. (Pubitemid 18036735)
9. BolchWE,Shah AP, Watchman CJ, JokischDW, PattonPW, Rajon DA, Zankl M, Petoussi-Henss N, Eckerman KF. 2007. Skeletal absorbed fractions for electrons in the adult male: Considerations of a revised 50-microm definition of the bone endosteum. Radiation Protection Dosimetry 127(1-4):169-173.
10. Brenner DJ, Doll R, Goodhead DT, Hall EJ, Land CE, Little JB, Lubin JH, Preston DL, Preston, RJ, Puskin JS, Ron E, Sachs RK, Samet JM, Setlow RB, Zaider M. 2003. Cancer risks attributable to low doses of ionizing radiation: Assessing what we really know. Proceedings of the National Academy of Sciences of the USA 100:13761-13766. (Pubitemid 37499140)
11. Cardis E, Gilbert ES, Carpenter L, Howe G, Kato I, Armstrong BK, Beral V, Cowper G, Douglas A, Fix J, Fry SA, Kaldor J, Lavé C, Salmon L, Smith PG, Voelz GL, Wiggs LD. 1995. Effects of low doses and low dose rates of external ionizing radiation: Cancer mortality among nuclear industry workers in three countries. Radiation Research 142:117-132.
12. Chang CM, Limanni A, Baker WH, Dobson ME, Kalinich JF, Jackson W, Patchen ML. 1995. Bone marrow and splenic granulocyte-macrophage colony-stimulating factor and transforming growth factor-beta mRNA levels in irradiated mice. Blood 86:2130-2136.
13. Colmone A. Amorim M. Pontier AL, Wang S. Jablonski E. Sipkins DA. 2008. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 322:1861-1865.
14. Cooper C, Harvey NC, Dennison EM, van Staa TP. 2006. Update on the epidemiology of Paget's disease of bone. Journal of Bone and Mineral Research 21(Suppl. 2):3-8.
15. Cristy M. 1981. Active bone marrow distribution as a function of age in humans. Physics in Medicine and Biology 26:389-400. (Pubitemid 11096423)
16. Curtis RE, Boice JD Jr, Stovall M, Bernstein L, Holowaty E, Karjalainen S, Langmark F, Nasca PC, Schwartz AG, Schymura MJ, Storm HH, Toogood P, Weyer P, Moloney WC. 1994. Relationship of leukemia risk to radiation dose following cancer of the uterine corpus. Journal of the National Cancer Institute 86:1315-1324. (Pubitemid 24276793)
17. Doll R, Wakeford R. 1997. Risk of childhood cancer from fetal irradiation. The British Journal of Radiology 70:130-139. (Pubitemid 27091013)
18. Eckerman KF, Stabin MG. 2000. Electron absorbed fractions and dose conversion factors for marrow and bone by skeletal regions. Health Physics 78:199-214. (Pubitemid 30061096)
19. Eliasson P, Jönsson J-I. 2010. The hematopoietic stem cell niche: Low in oxygen but a nice place to be. Journal of Cell Physiology 222:17-22.
20. Evans RD, Finkel AJ, Hasterlik RJ, Keane AT, Kolenkow RJ, Neal WR, Shanahan MM. 1969. Radiogenic tumors in the radium and mesothorium cases studied at M.I.T. In: Mays CW, et al. editors. Delayed effects of boneseeking radionuclides. Salt Lake City: University of Utah Press. pp 157-194.
21. Ford AM, Palmi C, Bueno C, Hong D, Cardus P, Knight D, Cazzaniga G, Enver T, Greaves M. 2009. The TEL-AML1 leukemia fusion gene dysregulates the TGF-ß pathway in early B lineage progenitor cells. The Journal of Clinical Investigation 119:826-836.
22. Ghadirian P, Fathie K, Emard JF. 2001. Epidemiology of bone cancer: An overview. Journal of Neurological and Orthopaedic Medicine and Surgery 21:8-16.
23. Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN, Steindler DA. 2005. Stem-like cells in bone sarcomas: Implications for tumorigenesis. Neoplasia 7:967-976.
24. Gnaiger E, Méndez G, Hand SC. 2000. High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proceedings of the National Academy of Sciences of the USA 97:11080-11085.
25. Gö ssner W. 1999. Pathology of radium-induced bone tumors: New aspects of histopathology and histogenesis. Radiation Research 152(Suppl.):12-15.
26. Gö ssner W. 2003 Target cells in internal dosimetry. Radiation Protection Dosimetry 105: 39-42. (Pubitemid 37167926)
27. Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T. 2006. Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. Journal of Cellular Physiology 207:331-339.
28. Greaves MF,Maia AT, Wiemels JL, Ford AM. 2003. Leukemia in twins: Lessons in natural history. Blood 102:2321-2333. (Pubitemid 37193565)
29. Guo W, Xu W, Huvos AG, Healey JH, Feng C. 1999. Comparative frequency of bone sarcomas among different racial groups. Chinese Medical Journal (English) 112:1101-1104.
30. Gurney JG, Swensen AR, Bulterys M. 1999. Malignant bone tumours. In: Ries LAG, Smith MA, Gurney JG, Linet M, Tamra T, Young JL, Bunin GR, editors. Cancer incidence and survival among children and adolescents: United States SEER Program 1975-1995. NIH Pub. No. 99-4649. Bethesda, MD: National Cancer Institute. pp 17-34.
31. Harrison JS. 2002. Oxygen saturation in the bone marrow of healthy volunteers. Blood 99:394.
32. Harrison JD, Muirhead CR. 2003. Quantitative comparisons of cancer induction in humans by internally deposited radionuclides and external radiation. International Journal of Radiation Biology 79:1-13. (Pubitemid 36140232)
33. Hashimoto J, Ohno I, Nakatsuka K, Yoshimura N, Takata S, Zamma M, Yabe H, Abe S, Terada M, Yoh K, Fukunaga M, Cooper C, Morii H, Yoshikawa H. 2006. Prevalence and clinical features of Paget's disease of bone in Japan. Journal of Bone and Mineral Metabolism 24:186-190.
34. Hayashi T, Kusunoki Y, Morishita Y, Nagamura H, Maki M, Kubo Y, Yamaoka M, Hayashi I, Yoshida K, Nakachi K. 2008. Acceleration of aging-associated increase in inflammatory markers and attenuation of the immune system among atomic-bomb survivors. Cytokine 43:255-256.
35. Hope KJ, Jin L, Dick JE. 2004. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in selfrenewal capacity. Nature Immunology 5:738-743. (Pubitemid 39023306)
36. Huvos AG. 1991. Bone tumors: Diagnosis, treatment and prognosis. Philadelphia: WB Saunders Co.
37. International Commission on Radiological Protection (ICRP Publication 11). 1968. A review of the radiosensitivity of the tissues in bone. Oxford: Elsevier.
38. International Commission on Radiological Protection (ICRP Publication 23). 1975. Reference man: Anatomical, physiological and metabolic characteristics. Oxford: Elsevier.
39. International Commission on Radiological Protection (ICRP Publication 30). 1979/81. Limits for intakes of radionuclides by workers. Oxford: Elsevier.
40. International Commission on Radiological Protection (ICRP Publication 56). 1989. Age-dependent doses to members of the public from intake of radionuclides. Oxford: Elsevier.
41. International Commission on Radiological Protection (ICRP Publication 70). 1995. Basic anatomical and physiological data for use in radiological protection: The skeleton. Oxford: Elsevier.
42. International Commission on Radiological Protection (ICRP Publication 88). 2001. Doses to the embryo and fetus from intakes of radionuclides by the mother ICRP. Oxford: Elsevier.
43. International Commission on Radiological Protection (ICRP Publication 90). 2003. Biological effects after prenatal irradiation (embryo and fetus). Oxford: Elsevier.
44. International Commission on Radiological Protection (ICRP Publication 103). 2007. Recommendations of the ICRP. Oxford: Elsevier.
45. Iikuni N, Kwan Lam QL, Lu L, Matarese G, Cava ALA. 2008. Leptin and inflammation. Current Immunology Reviews 10:70-79.
46. Ishikawa Y, Wada I, Fukumoto F. 2001. Alpha-particle carcinogenesis in Thorotrast patients: Epidemiology, dosimetry, pathology, and molecular analysis. Journal of Environmental Pathology, Toxicology and Oncology 20:311-315. (Pubitemid 34052128)
47. Ishikawa F, Yoshida S, Saito Y, Hijikata A, Kitamura H, Tanaka S, Nakamura R, Tanaka T, Tomiyama H, Saito N, Fukata M, Miyamoto T, Lyons B, Ohshima K, Uchida N, Taniguchi S, Ohara O, Akashi K, Harada M, Shultz LD. 2007. Chemotherapy- resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nature Biotechnology 25:1315-1321. (Pubitemid 350076512)
48. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, Gotlib J, Li K, Manz MG, Keating A, Sawyers CL, Weissman IL. 2004. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. The New England Journal of Medicine 351:657-667. (Pubitemid 39063268)
49. Jobling MF, Mott JD, Finnegan MT, Jurukovski V, Erickson AC, Walian PJ, Taylor SE, Ledbetter S, Lawrence CM, Rifkin DB, Barcellos-Hoff MH. 2006. Isoform-specific activation of latent transforming growth factor beta (LTGF-beta) by reactive oxygen species. Radiation Research 166:839-848. (Pubitemid 44888249)
50. Kadhim MA, Moore SR, Goodwin EH. 2004. Interrelationships amongst radiation-induced genomic instability, bystander effects, and the adaptive response. Mutation Research 568:21-32. (Pubitemid 39458293)
51. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. 2007. Tumor growth need not be driven by rare cancer stem cells. Science 317:337. (Pubitemid 47106366)
52. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109-1121. (Pubitemid 40884400)
53. Kiel MJ, Radice GL, Morrison SJ. 2007. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 1:127-129.
54. Koschmieder S, Hofmann WK, Kunert J, Wagner S, Ballas K, Seipelt G, Hoelzer D, Ottmann OG, Kalina U. 2001. TGF beta-induced SMAD2 phosphorylation predicts inhibition of thymidine incorporation in CD34cells from healthy donors, but not from patients with AML after MDS. Leukemia 15:942-949. (Pubitemid 32529895)
55. Kopp HG, Avecilla ST, Hooper AT, Rafii S. 2005. The bone marrow vascular niche: Home of HSC differentiation and mobilization. Physiology (Bethesda) 20:349-356. (Pubitemid 41457400)
56. Kuramoto K, Ban S, Oda K, Tanaka H, Kimura A, Suzuki G. 2002. Chromosomal instability and radiosensitivity in myelodyspastic cells. Leukemia 16:2253-2258. (Pubitemid 35339333)
57. Leenhouts HP, Brugmans MJP. 2000. An analysis of bone and head sinus cancers in radium dial painters using a twomutation carcinogenesis model. Journal of Radiological Protection 20:169-188. (Pubitemid 30352914)
58. Leggett RW. 1985. A model of the retention, translocation and excretion of systemic Pu. Health Physics 49:1115-1137. (Pubitemid 16178648)
59. Little MP. 2001. Comparison of the risks of cancer incidence and mortality following radiation therapy for benign and malignant disease with the cancer risks observed in the Japanese Atomic bomb survivors. International Journal of Radiation Biology 77:431-464. (Pubitemid 32281126)
60. Little MP, Weiss HA, Boice JD, Darby SC, Day NE, Muirhead CR. 1999. Risks of leukemia in Japanese atomic bomb survivors, in women treated for cervical cancer, and in patients treated for ankylosing spondylitis. Radiation Research 152:280-292. (Pubitemid 29413664)
61. Lloyd EL, Henning CB. 1983. Cells at risk for the production of bone tumors in radium exposed individuals: An electron microscope study. Health Physics 44 (Suppl. 1):135-148.
62. Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, Côté D, Rowe DW, Lin CP, Scadden DT. 2009. Live-animal tracking of individual hematopoietic stem/progenitor cells in their niche. Nature 457:92-96.
63. Lord BI. 1990. The architecture of bone marrow cell populations. The International Journal of Cell Cloning 8:317-331. (Pubitemid 20313340)
64. Lorimore SA, McIlrath JM, Coates PJ, Wright EG. 2005. Chromosomal instability in unirradiated hemopoietic cells resulting from a delayed in vivo bystander effect of gamma radiation. Cancer Research 65:5668-5673. (Pubitemid 40911168)
65. Mahmud N, Devine SM, Weller KP, Parmar S, Sturgeon C, Nelson MC, Hewett T, Hoffman R. 2001. The relative quiescence of hematopoietic stem cells in nonhuman primates. Blood 97:3061-3068.
66. Martin M, Lefaix J, Delanian S. 2000. TGF-b1 and radiation fibrosis: A master switch and a specific therapeutic target? International Journal of Radiation Oncology Biology Physics 47:277-290. (Pubitemid 30236366)
67. Medinger M, Mross K. 2010. Clinical trials with anti-angiogenic agents in hematological malignancies. Journal of Angiogenesis Research. 2:10 (doi:10.1186/2040-2384-2-10).
68. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B. 2004. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: The role of PPAR-g2 transcription factor and TGF-b/BMP signaling pathways. Aging Cell 3:379-389. (Pubitemid 40246708)
69. Moore KA, Lemischka IR. 2006. Stem cells and their niches. Science 311:1880-1885.
70. Mori T, Machinami R, Hatakeyama S, Fuktomi K, Kato Y, Akahi M, Fukmoto M, Aoki I. 2005. The 2002 results of the first series of follow-up studies on Japanese Thorotrast patients and their relationships to autopsy series. In: Oeh U, Roth P, Paretzke HG, editors. Health effects of internally deposited radionuclides: Emphasis on radium, thorium, uranium and their daughter products. Proc. HEIR 2004 Neuherberg: GSF - Forschungszentrum. pp 31-46.
71. Murphey MD, Robbin MR, McRae GA, Flemming DJ, Temple HT, Kransdorf MJ. 1997. The many faces of osteosarcoma. Radiographics 17:1205-1231.
72. Muschler GF, Nitto HJ, Boehm CA, Easley KA. 2001. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. Journal of Orthopaedic Research 19:117-125. (Pubitemid 32288644)
73. Muschler GF, Midura RJ, Nakamoto C. 2003. Practical modeling concepts for connective tissue stem cell and progenitor compartment kinetics. Journal of Biomedicine and Biotechnology 2003:170-193.
74. Nagasawa T. 2006. Microenvironmental niches in the bone marrow required for B-cell development. Nature Reviews Immunology 6:107-116. (Pubitemid 43361586)
75. Nekolla EA, Walsh L, Schottenhammer G, Spiess H. 2005. Malignancies in patients treated with high doses of 224Ra. In: Oeh U, Roth P, Paretzke HG, editors. Health effects of internally deposited radionuclides: Emphasis on radium, thorium, uranium and their daughter products. Proc. HEIR 2004 Neuherberg: GSF - Forschungszentrum. pp 67-74.
76. Nie H, Richardson RB. 2009. Radiation dose to trabecular bone marrow stem cells from 3H, 14C, and selected a-emitters incorporated in bone remodelling compartment. Physics in Medicine and Biology 54:963-979.
77. Nijnik A, Woodbine L, Marchetti C, Dawson S, Lambe T, Liu C, Rodrigues NP, Crockford TL, Cabuy E, Vindigni A, Enver T, Bell JI, Slijepcevic P, Goodnow CC, Jeggo PA. Cornall RJ. 2007. DNA repair is limiting for hematopoietic stem cells during ageing. Nature 447:686-690. (Pubitemid 46889732)
78. Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE. 1999. Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. Journal of Bone and Mineral Metabolism 17:171-177. (Pubitemid 29403926)
79. National Radiological Protection Board (NRPB). 2003. Risk of leukemia and related malignancies following radiation exposure: Estimated for the UK population Documents of the NRPB, 14,1 119S. Chilton, Didcot: NRPB.
80. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. 2006. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metabolism 3:187-197.
81. Parkin DM, Stiller CA, Nectoux J. 1993. International variations in the incidence of childhood bone tumours. International Journal of Cancer 53:371-376. (Pubitemid 23047882)
82. Parmar K, Mauch P, Vergilio JA, Sackstein R, Brown JD. 2007. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proceedings of the National Academy of Sciences of the USA 104:5431-5436. (Pubitemid 47175697)
83. Passegué E, Jamieson CH, Ailles LE, Weissman IL. 2003. Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proceedings of the National Academy of Sciences of the USA 100 (Suppl. 1):11842-11849. (Pubitemid 37205893)
84. Pierce DA, Vaeth M, Cologne JB. 2008. Allowance for random dose estimation errors in atomic bomb survivor studies: A revision. Radiation Research 170:118-126. (Pubitemid 351931193)
85. Pierce DA, Shimizu Y, Preston DL, Vaeth M, Mabuchi K. 1996. Studies of the mortality of atomic bomb survivors. Report 12, Part I. Cancer: 1950-1990. Radiation Research 146:1-27. (Pubitemid 26230829)
86. Pool RR, Morgan JP, Parks NJ, Farnham JE, Littman MS. 1983. Comparative pathogenesis of radium-induced intracortical bone lesions in humans and beagles. Health Physics 44(Suppl. 1):155-177.
87. Preston DL, Kusumi S, Tomonaga M, Izumi S, Ron E, Kuramoto A, Kamada N, Dohy H, Matsuo T, Nonaka H, Thompson DE, Soda M, Mabuchi K. 1994. Cancer incidence in atomic bomb survivors. Part III. Leukemia, lymphoma and multiple myeloma, 1950-1987. Radiation Research 137(Suppl. 2):S68- 97; Erratum: Radiation Research 139:129. (Pubitemid 24060247)
88. Preston DL, Ron E, Tokuoka S, Funamoto S, Nishi N, Soda M, Mabuchi K, Kodama K. 2007. Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiation Research 168:1-64. (Pubitemid 351292925)
89. Priest ND, Freemont A, Humphreys JA, Kathren RL. 1995. Histopathology and 241Am microdistribution in skeletal USTER Case 246. Health Physics 69:330-337.
90. Reya T, Morrison SJ, Clarke MF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105-111.
91. Richardson RB, Eatough JP, Henshaw DL. 1991. Dose to red bone marrow from natural radon and thoron exposure. The British Journal of Radiology 64:608-624.
92. Richardson RB, Dubeau J. 2003. Monte Carlo determination of age-dependent steady-state dose to red bone marrow and bone from 14C exposure. Radiation Protection Dosimetry 103:5-18. (Pubitemid 36124081)
93. Richardson RB, Nie HL, Chettle DR. 2007. Monte Carlo simulation of trabecular bone remodelling and absorbed dose coefficients for tritium and 14C. Radiation Protection Dosimetry 127:158-162.
94. Richardson RB. 2008. Age-dependent radiation effects to normal and diseased coronary arteries - part 3: Oxygen effect and its implications on high- and low-LET dose. International Journal of Radiation Biology 84:858-865.
95. Richardson RB. 2009a. Factors that elevate the internal radionuclide and chemical retention, dose and health risks to infants and children in a radiological-nuclear emergency. Radiation Protection Dosimetry 134:167-180.
96. Richardson RB. 2009b. Ionizing radiation and aging: Rejuvenating an old idea. Aging 1:887-902.
97. Richardson RB. 2010. A physiological skeletal model for radionuclide and stable element biokinetics in children and adults. Health Physics 99:471-482.
98. Richardson DB, Wing S, Schroeder J, Schmitz-Feuerhake I, Hoffmann W. 2005. Ionizing radiation and chronic lymphocytic leukemia. Environmental Health Perspectives 113:1-5.
99. Ries LAG, Melbert D, Krapcho M, Mariotto A, Miller BA, Feuer EJ, Clegg L, Horner MJ, Howlader N, Eisner MP, Reichman M, Edwards BK. 2007. SEER Cancer Statistics Review, 1975-2004. Bethesda, MD: National Cancer Institute. Accessed 10 October 2007 from the website: http://seer.cancer.gov/csr/1975-2004/
100. Rodríguez-Jiménez FJ, Moreno-Manzano V, Lucas-Dominguez R, Sánchez-Puelles JM. 2008. Hypoxia causes downregulation of mismatch repair system and genomic instability in stem cells. Stem Cells 26:2052-2062.
101. Rowland RE, Stehney AF, Lucas HF. 1983. Dose-response relationships for radium-induced sarcomas. Health Physics 44(Suppl. 1):15-31.
102. Schajowicz F, Santini Araujo E, Berenstein M. 1983. Sarcoma complicating Paget's disease of bone. A clinicopathological study of 62 cases. Journal of Bone and Joint Surgery - British Volume 65:299-307.
103. Schofield R. 1978. The relationship between the spleen colonyforming cell and the hemopoietic stem cells. A hypothesis. Blood Cells 4:7-25. (Pubitemid 8376317)
104. Shilnikova NS, Preston DL, Ron E, Gilbert ES, Vassilenko EK, Romanov SA, Kuznetsova IS, Sokolnikov ME, Okatenko PV, Kreslov VV, Koshurnikova NA. 2003. Cancer mortality among workers at the Mayak nuclear complex. Radiation Research 159:787-798. (Pubitemid 36676872)
105. Shuryak I, Sachs RK, Hlatky L, Hlatky L, Little MP, Hahnfeldt P, Brenner DJ. 2006. Radiation-induced leukemia at doses relevant to radiation therapy: Modeling mechanisms and estimating risks. Journal of the National Cancer Institute 98:1794-1806. (Pubitemid 46017931)
106. Sipkins DA, Wei X, Wu JW, Runnels JM, Côté D, Means TK, Luster AD, Scadden DT, Lin CP. 2005. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 435:969-973. (Pubitemid 40896324)
107. Smith MA, Ries LAG, Gurney JG, Ross JA. 1999. Leukemia. In: Ries LAG, Smith MA, Gurney JG, Linet M, Tamra T, Young JL, Bunin GR, editors. Cancer incidence and survival among children and adolescents: United States SEER Program 1975- 1995, NIH Pub. No. 99-4649 Bethesda, MD: National Cancer Institute. pp 17-34.
108. Spiers FW, Beddoe AH. 1983. Sites of incidence of osteosarcoma in the long bones of man and the beagle. Health Physics 44(Suppl. 1):49-64.
109. Spiers FW, Lucas HF, Rundo J, Anast GA. 1983. Leukemia incidence in the U.S. dial workers. Health Physics 44(Suppl. 1):65-72.
110. Spiess H. 1969. 224Ra-induced tumors in children and adults. In: Mays CW, Jee WSS, Lloyd RD, Stover BJ, Dougherty JH, Taylor GN editors. Delayed effects of bone-seeking radionuclides. Salt Lake City: University of Utah Press. pp 227- 243.
111. Streffer C. 2009. Radiological protection: Challenges and fascination of biological research. Strahlenschutzpraxis 2:(ISSN 0947-434 X).
112. Sugiyama T, Kohara H, Noda M, Nagasawa T. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12- CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977-988. (Pubitemid 44894948)
113. Thoday JM, Read J. 1949. Effect of oxygen on the frequency of chromosomal aberrantions produced by X-rays. Nature 160:608-609.
114. Tsukasaki K, Iwanaga M, Tomonaga M. 2007. Late haematological effects in atomic bomb survivors. International Congress Series 1299:67-72.
115. Tucker MA, D'Angio GJ, Boice JD Jr, Strong LC, Li FP, Stovall M, Stone BJ, Green DM, Lombardi F, Newton W, Hoover RN, Fraumeni JF. 1987. Bone sarcomas linked to radiotherapy and chemotherapy in children. The New England Journal of Medicine 317:588-593. (Pubitemid 17126781)
116. Unni K.K. 1996.Dahlin's bone tumours.General aspects and data on 11,087 cases. 5th ed. Philadelphia,New York: Lippincott-Raven.
117. Vacanti C. 2004. Cells for building. The Scientist 22-23. (Pubitemid 39636131)
118. van Kaick G, Wesch H. 2005. The national Thorotrast studies in comparison. In: Oeh U, Roth P, Paretzke HG, editors. Health effects of internally deposited radionuclides: Emphasis on radium, thorium, uranium and their daughter products. Proc. HEIR 2004 Neuherberg: GSF - Forschungszentrum. pp 17-20.
119. Visfeldt J, Andersson M. 1995. Pathoanatomical aspects of malignant haematological disorders among Danish patients exposed to thorium dioxide. Acta Pathologica, Microbiologica et Immunologica Scandinavica 103:29-36.
120. Weiss HA, Darby SC, Fearn T, Doll R. 1995. Leukemia mortality after X-ray treatment for ankylosing spondylitis. Radiation Research 142:1-11.
121. Wick MR, Siegal GP, Unni KK, Mcleod RA, Greditzer HG. 1981. Sarcomas of bone complicating osteitis deformans (Paget's disease), 50 years experience. The American Journal of Surgical Pathology 5:47-59. (Pubitemid 11142391)
122. Wick RR, Nekolla EA. 2005. Long term investigation of late effects in ankylosing spodylitis patients treated with 224Ra. In: Oeh U, Roth P, Paretzke HG, editors. Health effects of internally deposited radionuclides: Emphasis on radium, thorium, uranium and their daughter products. Proc. HEIR 2004 Neuherberg: GSF - Forschungszentrum. pp 75- 81.
123. Xie Y, Yin T, Wiegraebe W, He XC, Miller D, Stark D, Perko K, Alexander R, Schwartz J, Grindley JC, Park J, Haug JS, Wunderlich JP, Li H, Zhang S, Johnson T, Feldman RA, Li L. 2009. Detection of functional hematopoietic stem cell niche using real-time imaging. Nature 457:97-101.