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Redox Regulation of Stem Cell Compartments: The Convergence of Radiation-Induced Normal Tissue Damage and Oxidative Stress

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Oxidative Stress in Cancer Biology and Therapy

Abstract

The redox environment impacts normal stem cell niches throughout the body. Hematopoietic, muscle, and neural stem cell compartments respond to changes in reactive oxygen (ROS) and nitrogen (RNS) species by triggering signaling networks that impact cellular proliferation, survival, and differentiation. Work from many labs including our own has found that irradiation can trigger acute and chronic increases in oxidative stress. Low dose and/or protracted dose rates can elicit radioadaptive changes that have beneficial effects on proliferation and survival while influencing the development lineage-specific cell fates. Higher doses and dose rates have been found to impede the regeneration of irradiated tissues, through the depletion and/or damage of endogenous stem cell pools, and by promoting the onset and persistence of secondary reactive processes involving oxidative stress and inflammatory cytokines. Increasing evidence suggests that these important stem cell pools are differentially protected from DNA damaging agents compared to their immediate progeny (i.e., precursor/progenitor cells) due to enhanced DNA repair, antioxidant status, and reduced cell cycle activity. Thus, many of the adverse effects of irradiation on normal tissue are the consequence of damage to the rapidly expanding pool of precursor cells derived from asymmetric cell division. Irradiation of the bone marrow impairs the health of bone by promoting osteoclastogenesis (osteoclast-mediated bone resorption) and inhibiting osteoblastogenesis (osteoblast-mediated bone formation), with the net effect of reducing bone mass and structural integrity. Irradiation of the skeletal musculature impairs myogenesis (formation of muscle tissue) by damaging satellite cells (i.e., muscle stem cells) and reducing proproliferative levels of nitric oxide. In the brain, irradiation depletes neural stem and precursor cells and leads to persistent increases in ROS/RNS and inflammatory cytokines that inhibit neurogenesis (formation of new neurons and glia) and adversely impact cognition. In each of these foregoing cases, interventions targeted to reduce specific reactive species can attenuate the adverse effects of radiation exposure and point to the importance of understanding the interplay between endogenous stem cell niches and the microenvironmental redox state.

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References

  1. Fike JR, Rosi S, Limoli CL (2009) Neural precursor cells and central nervous system radiation sensitivity. Semin Radiat Oncol 19(2):122–132

    Article  PubMed  Google Scholar 

  2. Fike JR, Rola R, Limoli CL (2007) Radiation response of neural precursor cells. Neurosurg Clin N Am 18(1):115–127

    Article  PubMed  Google Scholar 

  3. Butler JM, Rapp SR, Shaw EG (2006) Managing the cognitive effects of brain tumor radiation therapy. Curr Treat Options Oncol 7(6):517–523

    Article  PubMed  Google Scholar 

  4. Meyers CA, Brown PD (2006) Role and relevance of neurocognitive assessment in clinical trials of patients with CNS tumors. J Clin Oncol 24(8):1305–1309

    Article  PubMed  Google Scholar 

  5. Raber J et al (2004) Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162(1):39–47

    Article  PubMed  CAS  Google Scholar 

  6. Roman DD, Sperduto PW (1995) Neuropsychological effects of cranial radiation: current knowledge and future directions. Int J Radiat Oncol Biol Phys 31(4):983–998

    Article  PubMed  CAS  Google Scholar 

  7. Surma-aho O et al (2001) Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 56(10):1285–1290

    Article  PubMed  CAS  Google Scholar 

  8. Cucinotta FA, Durante M (2006) Cancer risk from exposure to galactic cosmic rays: implications for space exploration by human beings. Lancet Oncol 7(5):431–435

    Article  PubMed  CAS  Google Scholar 

  9. Durante M, Cucinotta FA (2008) Heavy ion carcinogenesis and human space exploration. Nat Rev Cancer 8(6):465–472

    Article  PubMed  CAS  Google Scholar 

  10. Giedzinski E, Rola R, Fike JR, Limoli CL (2005) Efficient production of reactive oxygen species in neural precursor cells after exposure to 250 MeV protons. Radiat Res 164(4 Pt 2):540–544

    Article  PubMed  CAS  Google Scholar 

  11. Limoli CL, Giedzinski E, Baure J, Rola R, Fike JR (2006) Altered growth and radiosensitivity in neural precursor cells subjected to oxidative stress. Int J Radiat Biol 82(9):640–647

    Article  PubMed  CAS  Google Scholar 

  12. Limoli CL, Giedzinski E, Baure J, Rola R, Fike JR (2007) Redox changes induced in hippocampal precursor cells by heavy ion irradiation. Radiat Environ Biophys 46(2):167–172

    Article  PubMed  CAS  Google Scholar 

  13. Limoli CL et al (2004) Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat Res 161(1):17–27

    Article  PubMed  CAS  Google Scholar 

  14. Limoli CL et al (2004) Cell-density-dependent regulation of neural precursor cell function. Proc Natl Acad Sci USA 101(45):16052–16057

    Article  PubMed  CAS  Google Scholar 

  15. Wardman P (2008) Use of the dichlorofluorescein assay to measure “reactive oxygen species”. Radiat Res 170(3):406–407

    Article  PubMed  CAS  Google Scholar 

  16. Mizumatsu S et al (2003) Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 63(14):4021–4027

    PubMed  CAS  Google Scholar 

  17. Rola R et al (2007) Lack of extracellular superoxide dismutase (EC-SOD) in the microenvironment impacts radiation-induced changes in neurogenesis. Free Radic Biol Med 42(8):1133–1145, discussion 1131–1132

    Article  PubMed  CAS  Google Scholar 

  18. Fishman K et al (2009) Radiation-induced reductions in neurogenesis are ameliorated in mice deficient in CuZnSOD or MnSOD. Free Radic Biol Med 47(10):1459–1467

    Article  PubMed  CAS  Google Scholar 

  19. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8(9):955–962

    Article  PubMed  CAS  Google Scholar 

  20. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302(5651):1760–1765

    Article  PubMed  CAS  Google Scholar 

  21. Dent P et al (2003) Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat Res 159(3):283–300

    Article  PubMed  CAS  Google Scholar 

  22. Gius D, Spitz DR (2006) Redox signaling in cancer biology. Antioxid Redox Signal 8(7–8):1249–1252

    Article  PubMed  CAS  Google Scholar 

  23. Mikkelsen RB, Wardman P (2003) Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 22(37):5734–5754

    Article  PubMed  CAS  Google Scholar 

  24. Kim J, Wong PK (2009) Loss of ATM impairs proliferation of neural stem cells through oxidative stress-mediated p38 MAPK signaling. Stem Cell 27(8):1987–1998

    Article  CAS  Google Scholar 

  25. Kim J, Wong PK (2009) Oxidative stress is linked to ERK1/2-p16 signaling-mediated growth defect in ATM-deficient astrocytes. J Biol Chem 284(21):14396–14404

    Article  PubMed  CAS  Google Scholar 

  26. Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R, Mikkelsen RB (2001) Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 61(10):3894–3901

    PubMed  CAS  Google Scholar 

  27. Venkatachalam P et al (2008) Regulation of normal cell cycle progression by flavin-containing oxidases. Oncogene 27(1):20–31

    Article  PubMed  CAS  Google Scholar 

  28. Leach JK, Black SM, Schmidt-Ullrich RK, Mikkelsen RB (2002) Activation of constitutive nitric-oxide synthase activity is an early signaling event induced by ionizing radiation. J Biol Chem 277(18):15400–15406

    Article  PubMed  CAS  Google Scholar 

  29. Boveris A & Cadenas E (1982) Production of superoxide radicals and hydrogen peroxide in mitochondria. In: OL W (ed) Superoxide dismutase, vol II. CRC Press, Boca Raton, FL, pp 15–30

    Google Scholar 

  30. Lewen A, Matz P, Chan PH (2000) Free radical pathways in CNS injury. J Neurotrauma 17(10):871–890

    Article  PubMed  CAS  Google Scholar 

  31. Wardman P, Candeias LP (1996) Fenton chemistry: an introduction. Radiat Res 145(5):523–531

    Article  PubMed  CAS  Google Scholar 

  32. Chan PH (1994) Oxygen radicals in focal cerebral ischemia. Brain Pathol 4(1):59–65

    Article  PubMed  CAS  Google Scholar 

  33. Peuchen S et al (1997) Interrelationships between astrocyte function, oxidative stress and antioxidant status within the central nervous system. Prog Neurobiol 52(4):261–281

    Article  PubMed  CAS  Google Scholar 

  34. Smith KJ, Kapoor R, Felts PA (1999) Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol 9(1):69–92

    Article  PubMed  CAS  Google Scholar 

  35. Irani K et al (1997) Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275(5306):1649–1652

    Article  PubMed  CAS  Google Scholar 

  36. Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T (2000) Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol 20(19):7311–7318

    Article  PubMed  CAS  Google Scholar 

  37. Menon SG et al (2003) Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Res 63(9):2109–2117

    PubMed  CAS  Google Scholar 

  38. Sarsour EH, Agarwal M, Pandita TK, Oberley LW, Goswami PC (2005) Manganese superoxide dismutase protects the proliferative capacity of confluent normal human fibroblasts. J Biol Chem 280(18):18033–18041

    Article  PubMed  CAS  Google Scholar 

  39. Tofilon PJ, Fike JR (2000) The radioresponse of the central nervous system: a dynamic process. Radiat Res 153(4):357–370

    Article  PubMed  CAS  Google Scholar 

  40. Ishii J et al (2007) The free-radical scavenger edaravone restores the differentiation of human neural precursor cells after radiation-induced oxidative stress. Neurosci Lett 423(3):225–230

    Article  PubMed  CAS  Google Scholar 

  41. Madhavan L, Ourednik V, Ourednik J (2008) Neural stem/progenitor cells initiate the formation of cellular networks that provide neuroprotection by growth factor-modulated antioxidant expression. Stem Cell 26(1):254–265

    Article  CAS  Google Scholar 

  42. Park M et al (2009) 2-Deoxy-d-glucose protects neural progenitor cells against oxidative stress through the activation of AMP-activated protein kinase. Neurosci Lett 449(3):201–206

    Article  PubMed  CAS  Google Scholar 

  43. Sharma RK, Zhou Q, Netland PA (2008) Effect of oxidative preconditioning on neural progenitor cells. Brain Res 1243:19–26

    Article  PubMed  CAS  Google Scholar 

  44. Wolff S (1998) The adaptive response in radiobiology: evolving insights and implications. Environ Health Perspect 106(Suppl 1):277–283

    Article  PubMed  Google Scholar 

  45. Ko M, Lao XY, Kapadia R, Elmore E, Redpath JL (2006) Neoplastic transformation in vitro by low doses of ionizing radiation: role of adaptive response and bystander effects. Mutat Res 597(1–2):11–17

    PubMed  CAS  Google Scholar 

  46. Mitchell SA, Marino SA, Brenner DJ, Hall EJ (2004) Bystander effect and adaptive response in C3H 10 T(1/2) cells. Int J Radiat Biol 80(7):465–472

    Article  PubMed  CAS  Google Scholar 

  47. Preston RJ (2005) Bystander effects, genomic instability, adaptive response, and cancer risk assessment for radiation and chemical exposures. Toxicol Appl Pharmacol 207(2 Suppl):550–556

    Article  PubMed  CAS  Google Scholar 

  48. Morgan WF (2006) Will radiation-induced bystander effects or adaptive responses impact on the shape of the dose response relationships at low doses of ionizing radiation? Dose Response 4(4):257–262

    Article  PubMed  CAS  Google Scholar 

  49. Azzam EI, Raaphorst GP, Mitchel RE (1994) Radiation-induced adaptive response for protection against micronucleus formation and neoplastic transformation in C3H 10 T1/2 mouse embryo cells. Radiat Res 138(1 Suppl):S28–S31

    Article  PubMed  CAS  Google Scholar 

  50. Limoli CL, Kaplan MI, Giedzinski E, Morgan WF (2001) Attenuation of radiation-induced genomic instability by free radical scavengers and cellular proliferation. Free Radic Biol Med 31(1):10–19

    Article  PubMed  CAS  Google Scholar 

  51. Spitz DR, Azzam EI, Li JJ, Gius D (2004) Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Rev 23(3–4):311–322

    Article  PubMed  CAS  Google Scholar 

  52. Bubici C, Papa S, Pham CG, Zazzeroni F, Franzoso G (2006) The NF-kappaB-mediated control of ROS and JNK signaling. Histol Histopathol 21(1):69–80

    PubMed  CAS  Google Scholar 

  53. de Toledo SM et al (2006) Adaptive responses to low-dose/low-dose-rate gamma rays in normal human fibroblasts: the role of growth architecture and oxidative metabolism. Radiat Res 166(6):849–857

    Article  PubMed  Google Scholar 

  54. Elmore E et al (2008) Low doses of very low-dose-rate low-LET radiation suppress radiation-induced neoplastic transformation in vitro and induce an adaptive response. Radiat Res 169(3):311–318

    Article  PubMed  CAS  Google Scholar 

  55. Guo G et al (2003) Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses. Mol Cell Biol 23(7):2362–2378

    Article  PubMed  CAS  Google Scholar 

  56. Oberley LW (2005) Mechanism of the tumor suppressive effect of MnSOD overexpression. Biomed Pharmacother 59(4):143–148

    Article  PubMed  CAS  Google Scholar 

  57. Zhang Y, Smith BJ, Oberley LW (2006) Enzymatic activity is necessary for the tumor-suppressive effects of MnSOD. Antioxid Redox Signal 8(7–8):1283–1293

    Article  PubMed  CAS  Google Scholar 

  58. Kaewpila S, Venkataraman S, Buettner GR, Oberley LW (2008) Manganese superoxide dismutase modulates hypoxia-inducible factor-1 alpha induction via superoxide. Cancer Res 68(8):2781–2788

    Article  PubMed  CAS  Google Scholar 

  59. Huang TT et al (1999) The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann N Y Acad Sci 893:95–112

    Article  PubMed  CAS  Google Scholar 

  60. Slemmer JE, Shacka JJ, Sweeney MI, Weber JT (2008) Antioxidants and free radical scavengers for the treatment of stroke, traumatic brain injury and aging. Curr Med Chem 15(4):404–414

    Article  PubMed  CAS  Google Scholar 

  61. Valko M et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84

    Article  PubMed  CAS  Google Scholar 

  62. Hu D et al (2007) Hippocampal long-term potentiation, memory, and longevity in mice that overexpress mitochondrial superoxide dismutase. Neurobiol Learn Mem 87(3):372–384

    Article  PubMed  CAS  Google Scholar 

  63. Kishida KT, Klann E (2007) Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxid Redox Signal 9(2):233–244

    Article  PubMed  CAS  Google Scholar 

  64. Levin ED et al (1998) Molecular manipulations of extracellular superoxide dismutase: functional importance for learning. Behav Genet 28(5):381–390

    Article  PubMed  CAS  Google Scholar 

  65. Raber J, et al (2009) Irradiation enhances hippocampus-dependent cognition in mice deficient in extracellular superoxide dismutase. Hipppocampus (in press)

    Google Scholar 

  66. Gori T, Forconi S (2005) The role of reactive free radicals in ischemic preconditioning – clinical and evolutionary implications. Clin Hemorheol Microcirc 33(1):19–28

    PubMed  CAS  Google Scholar 

  67. Yu BP, Chung HY (2006) Adaptive mechanisms to oxidative stress during aging. Mech Ageing Dev 127(5):436–443

    Article  PubMed  CAS  Google Scholar 

  68. Qutob SS et al (2006) Fractionated X-radiation treatment can elicit an inducible-like radioprotective response that is not dependent on the intrinsic cellular X-radiation resistance/sensitivity. Radiat Res 166(4):590–599

    Article  PubMed  CAS  Google Scholar 

  69. Cao L et al (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36(8):827–835

    Article  PubMed  CAS  Google Scholar 

  70. Cardenas A, Moro MA, Hurtado O, Leza JC, Lizasoain I (2005) Dual role of nitric oxide in adult neurogenesis. Brain Res Brain Res Rev 50(1):1–6

    Article  PubMed  CAS  Google Scholar 

  71. Gibbs SM (2003) Regulation of neuronal proliferation and differentiation by nitric oxide. Mol Neurobiol 27(2):107–120

    Article  PubMed  CAS  Google Scholar 

  72. Scharfman H et al (2005) Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol 192(2):348–356

    Article  PubMed  CAS  Google Scholar 

  73. Barkho BZ et al (2006) Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cell Dev 15(3):407–421

    Article  CAS  Google Scholar 

  74. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26(10):523–530

    Article  PubMed  CAS  Google Scholar 

  75. Jordan JD, Ma DK, Ming GL, Song H (2007) Cellular niches for endogenous neural stem cells in the adult brain. CNS Neurol Disord Drug Targets 6(5):336–341

    Article  PubMed  CAS  Google Scholar 

  76. Oberley LW, Oberley TD, Buettner GR (1980) Cell differentiation, aging and cancer: the possible roles of superoxide and superoxide dismutases. Med Hypotheses 6(3):249–268

    Article  PubMed  CAS  Google Scholar 

  77. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  PubMed  CAS  Google Scholar 

  78. Alameddine HS, Dehaupas M, Fardeau M (1989) Regeneration of skeletal muscle fibers from autologous satellite cells multiplied in vitro. An experimental model for testing cultured cell myogenicity. Muscle Nerve 12(7):544–555

    Article  PubMed  CAS  Google Scholar 

  79. Bischoff R (1975) Regeneration of single skeletal muscle fibers in vitro. Anat Rec 182(2):215–235

    Article  PubMed  CAS  Google Scholar 

  80. Fulle S, Belia S, Di Tano G (2005) Sarcopenia is more than a muscular deficit. Arch Ital Biol 143(3–4):229–234

    PubMed  CAS  Google Scholar 

  81. Rosenblatt JD, Yong D, Parry DJ (1994) Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 17(6):608–613

    Article  PubMed  CAS  Google Scholar 

  82. Tatsumi R, Allen RE (2004) Active hepatocyte growth factor is present in skeletal muscle extracellular matrix. Muscle Nerve 30(5):654–658

    Article  PubMed  CAS  Google Scholar 

  83. Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54(11):1177–1191

    Article  PubMed  CAS  Google Scholar 

  84. Ashton LA, Bruce W, Goldberg J, Walsh W (2000) Prevention of heterotopic bone formation in high risk patients post-total hip arthroplasty. J Orthop Surg (Hong Kong) 8(2):53–57

    Google Scholar 

  85. Balboni TA, Gobezie R, Mamon HJ (2006) Heterotopic ossification: pathophysiology, clinical features, and the role of radiotherapy for prophylaxis. Int J Radiat Oncol Biol Phys 65(5):1289–1299

    Article  PubMed  Google Scholar 

  86. Coventry MB, Scanlon PW (1981) The use of radiation to discourage ectopic bone. A nine-year study in surgery about the hip. J Bone Joint Surg Am 63(2):201–208

    PubMed  CAS  Google Scholar 

  87. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH (2008) Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cell 26(4):960–968

    Article  CAS  Google Scholar 

  88. Rietman JS et al (2004) Impairments, disabilities and health related quality of life after treatment for breast cancer: a follow-up study 2.7 years after surgery. Disabil Rehabil 26(2):78–84

    Article  PubMed  Google Scholar 

  89. Senkus-Konefka E, Jassem J (2006) Complications of breast-cancer radiotherapy. Clin Oncol (R Coll Radiol) 18(3):229–235

    Article  CAS  Google Scholar 

  90. Shamley DR et al (2007) Changes in shoulder muscle size and activity following treatment for breast cancer. Breast Cancer Res Treat 106(1):19–27

    Article  PubMed  Google Scholar 

  91. Stoltny T, Koczy B, Wawrzynek W, Miszczyk L (2007) Heterotopic ossification in patients after total hip replacement. Ortop Traumatol Rehabil 9(3):264–272

    PubMed  Google Scholar 

  92. Allen DL, Roy RR, Edgerton VR (1999) Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22(10):1350–1360

    Article  PubMed  CAS  Google Scholar 

  93. Allen DL, Monke SR, Talmadge RJ, Roy RR, Edgerton VR (1995) Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. J Appl Physiol 78(5):1969–1976

    PubMed  CAS  Google Scholar 

  94. Tatsumi R et al (2006) Satellite cell activation in stretched skeletal muscle and the role of nitric oxide and hepatocyte growth factor. Am J Physiol Cell Physiol 290(6):1487–1494

    Article  CAS  Google Scholar 

  95. Tatsumi R et al (2009) A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation. Am J Physiol Cell Physiol 296(4):922–929

    Article  CAS  Google Scholar 

  96. Baxter NN, Habermann EB, Tepper JE, Durham SB, Virnig BA (2005) Risk of pelvic fractures in older women following pelvic irradiation. JAMA 294(20):2587–2593

    Article  PubMed  CAS  Google Scholar 

  97. Grigoriadis AE, Heersche JN, Aubin JE (1988) Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone. J Cell Biol 106(6):2139–2151

    Article  PubMed  CAS  Google Scholar 

  98. Burger EH et al (1982) In vitro formation of osteoclasts from long-term cultures of bone marrow mononuclear phagocytes. J Exp Med 156(6):1604–1614

    Article  PubMed  CAS  Google Scholar 

  99. Martin T, Gooi JH, Sims NA (2009) Molecular mechanisms in coupling of bone formation to resorption. Crit Rev Eukaryot Gene Expr 19(1):73–88

    Article  PubMed  CAS  Google Scholar 

  100. Calvi LM et al (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425(6960):841–846

    Article  PubMed  CAS  Google Scholar 

  101. Mizoguchi T et al (2009) Identification of cell cycle-arrested quiescent osteoclast precursors in vivo. J Cell Biol 184(4):541–554

    Article  PubMed  CAS  Google Scholar 

  102. Cao JJ et al (2005) Aging increases stromal/osteoblastic cell-induced osteoclastogenesis and alters the osteoclast precursor pool in the mouse. J Bone Miner Res 20(9):1659–1668

    Article  PubMed  CAS  Google Scholar 

  103. Jilka RL et al (1998) Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 101(9):1942–1950

    Article  PubMed  CAS  Google Scholar 

  104. Greenberger JS, Epperly M (2009) Bone marrow-derived stem cells and radiation response. Semin Radiat Oncol 19(2):133–139

    Article  PubMed  Google Scholar 

  105. Anderson ND, Colyer RA, Riley LH Jr (1979) Skeletal changes during prolonged external irradiation: alterations in marrow, growth plate and osteoclast populations. Johns Hopkins Med J 145(3):73–83

    PubMed  CAS  Google Scholar 

  106. Kondo H, et al (2009) Oxidative stress and gamma radiation-induced cancellous bone loss with musculoskeletal disuse. J Appl Physiol (in press)

    Google Scholar 

  107. Wang D, Jang DJ (2009) Protein kinase CK2 regulates cytoskeletal reorganization during ionizing radiation-induced senescence of human mesenchymal stem cells. Cancer Res 69(20):8200–8207

    Article  PubMed  CAS  Google Scholar 

  108. Li J, Kwong DL, Chan GC (2007) The effects of various irradiation doses on the growth and differentiation of marrow-derived human mesenchymal stromal cells. Pediatr Transplant 11(4):379–387

    Article  PubMed  Google Scholar 

  109. Ma J et al (2007) Senescence-unrelated impediment of osteogenesis from Flk1+ bone marrow mesenchymal stem cells induced by total body irradiation and its contribution to long-term bone and hematopoietic injury. Haematologica 92(7):889–896

    Article  PubMed  Google Scholar 

  110. Kondo H et al (2007) Shared oxidative pathways in response to gravity-dependent loading and gamma-irradiation of bone marrow-derived skeletal cell progenitors. Radiats Biol Radioecol 47(3):281–285

    PubMed  CAS  Google Scholar 

  111. Matsumura S et al (1998) Changes in phenotypic expression of osteoblasts after X irradiation. Radiat Res 149(5):463–471

    Article  PubMed  CAS  Google Scholar 

  112. Kondo H et al (2009) Total-body irradiation of postpubertal mice with (137)Cs acutely compromises the microarchitecture of cancellous bone and increases osteoclasts. Radiat Res 171(3):283–289

    Article  PubMed  CAS  Google Scholar 

  113. Willey JS, et al. (2009) Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations. Bone (in press)

    Google Scholar 

  114. Yumoto K, et al. (2009) Short-term effects of whole body (56)Fe particle irradiation in combination with musculoskeletal disuse on bone cells. Radiat Res (in press)

    Google Scholar 

  115. Komarova SV, Ataullakhanov FI, Globus RK (2000) Bioenergetics and mitochondrial transmembrane potential during differentiation of cultured osteoblasts. Am J Physiol Cell Physiol 279(4):C1220–C1229

    PubMed  CAS  Google Scholar 

  116. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD (2007) Distribution of hematopoi­etic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA 104(13):5431–5436

    Article  PubMed  CAS  Google Scholar 

  117. Garrett IR et al (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85(3):632–639

    Article  PubMed  CAS  Google Scholar 

  118. Nilforoushan D, Gramoun A, Glogauer M, Manolson MF (2009) Nitric oxide enhances osteoclastogenesis possibly by mediating cell fusion. Nitric Oxide 21(1):27–36

    Article  PubMed  CAS  Google Scholar 

  119. Halleen JM et al (1999) Intracellular fragmentation of bone resorption products by reactive oxygen species generated by osteoclastic tartrate-resistant acid phosphatase. J Biol Chem 274(33):22907–22910

    Article  PubMed  CAS  Google Scholar 

  120. Bai XC et al (2005) Reactive oxygen species stimulates receptor activator of NF-kappaB ligand expression in osteoblast. J Biol Chem 280(17):17497–17506

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Office of Science (BER), US Department of Energy (DOE), Grant No. DE-FG02-09ER64798 to (CLL), National Aeronautics and Space Administration (NASA) Grant No. NNX09AK25G to (CLL) and NASA Grant #NNH04ZUU005N/RAD2004-000-0110 to (RKG), DOE-NASA Interagency Award #DE-SC0001507 to (RKG), American Cancer Society Grant #RSG-00-036-04-CNE to (CLL), and NIH Grant R01 NS46051 to (JRF).

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Authors and Affiliations

  1. Space Biosciences Division, NASA Ames Research Center, Moffett Field, CA, 94035-1000, USA

    Ruth K. Globus PhD

  2. Department of Orthopaedic Surgery, University of California, Irvine, CA, 92697-5399, USA

    Vincent Caiozzo PhD

  3. Department of Radiation Oncology, University of California, Irvine, CA, 92697-2695, USA

    Munjal Acharya PhD & Charles Limoli PhD

  4. Departments of Neurological Surgery and Radiation Oncology, Brain and Spinal Injury Center, University of California, San Francisco, CA, 94110-0899, USA

    John R. Fike PhD

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  1. Ruth K. Globus PhD
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  5. Charles Limoli PhD
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Editor information

Editors and Affiliations

  1. Free Radical & Radiation Biology, Graduate Program, University of Iowa, Iowa City, 52242, Iowa, USA

    Douglas R. Spitz

  2. Duluth Clinic, Radiation Oncology, University of Minnesota, East 3rd Street 400, Duluth, 55805, Minnesota, USA

    Kenneth J. Dornfeld

  3. James H. Quillen College of Medicine, Internal Medicine, East Tennessee State University, Johnson City, 37614, Tennessee, USA

    Koyamangalath Krishnan

  4. Radiation Oncology, Cancer Biology and Pediatrics, Vanderbilt Medical School, 21st Ave. 1161, Nashville, 37232, Tennessee, USA

    David Gius

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© 2012 Springer Science+Business Media, LLC

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Globus, R.K., Caiozzo, V., Acharya, M., Fike, J.R., Limoli, C. (2012). Redox Regulation of Stem Cell Compartments: The Convergence of Radiation-Induced Normal Tissue Damage and Oxidative Stress. In: Spitz, D., Dornfeld, K., Krishnan, K., Gius, D. (eds) Oxidative Stress in Cancer Biology and Therapy. Oxidative Stress in Applied Basic Research and Clinical Practice. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-61779-397-4_9

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