Experimental Hematology
Volume 36, Issue 9 , Pages 1143-1156.e3 , September 2008

Bone marrow sinusoidal endothelial cells undergo nonapoptotic cell death and are replaced by proliferating sinusoidal cells in situ to maintain the vascular niche following lethal irradiation

  • Xiao-Miao Li

      Affiliations

    • Department of Pediatrics, Division of Pediatric Hematology/Oncology, University of Florida, Gainesville, Fla., USA
  • ,
  • Zhongbo Hu

      Affiliations

    • Department of Pediatrics, Division of Pediatric Hematology/Oncology, University of Florida, Gainesville, Fla., USA
  • ,
  • Marda L. Jorgenson

      Affiliations

    • Department of Regenerative Medicine, University of Florida, Gainesville, Fla., USA
  • ,
  • John R. Wingard

      Affiliations

    • Department of Medicine Division of Blood and Marrow Transplantation, University of Florida, Gainesville, Fla., USA
  • ,
  • William B. Slayton

      Affiliations

    • Department of Pediatrics, Division of Pediatric Hematology/Oncology, University of Florida, Gainesville, Fla., USA
    • Corresponding Author InformationOffprint requests to: William B. Slayton, M.D., Department of Pediatrics, Division of Pediatric Hematology/Oncology, University of Florida Health Sciences Center, Box 100296, Gainesville, FL 32610

Received 11 June 2008 ,Revised 11 June 2008 ,Accepted 18 June 2008.

References 

  1. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121:1109–1121
  2. Avecilla ST, Hattori K, Heissig B, et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med. 2004;10:64–71
  3. Richardson P, Guinan E. Hepatic veno-occlusive disease following hematopoietic stem cell transplantation. Acta Haematol. 2001;106:57–68
  4. Seguchi M, Hirabayashi N, Fujii Y, et al. Pulmonary hypertension associated with pulmonary occlusive vasculopathy after allogeneic bone marrow transplantation. Transplantation. 2000;69:177–179
  5. Selby DM, Rudzki JR, Bayever ES, Chandra RS. Vasculopathy of small muscular arteries in pediatric patients after bone marrow transplantation. Hum Pathol. 1999;30:734–740
  6. Hale GA, Bowman LC, Rochester RJ, et al. Hemolytic uremic syndrome after bone marrow transplantation: clinical characteristics and outcome in children. Biol Blood Marrow Transplant. 2005;11:912–920
  7. Ohno E, Ohtsuka E, Iwashita T, et al. Hemolytic uremic syndrome following autologous peripheral blood stem cell transplantation in a patient with malignant lymphoma. Bone Marrow Transplant. 1997;19:1045–1047
  8. Pucci G, Martino M, Morabito F, et al. Thrombotic thrombocytopenic purpura: a rare late complication of allogeneic bone marrow transplantation. Haematologica. 1994;79:371–373
  9. Nurnberger W, Willers R, Burdach S, Gobel U. Risk factors for capillary leakage syndrome after bone marrow transplantation. Ann Hematol. 1997;74:221–224
  10. Narayan K, Juneja S, Garcia C. Effects of 5-fluorouracil or total-body irradiation on murine bone marrow microvasculature. Exp Hematol. 1994;22:142–148
  11. Narayan K, Cliff WJ. Morphology of irradiated microvasculature: a combined in vivo and electron-microscopic study. Am J Pathol. 1982;106:47–62
  12. Shirota T, Tavassoli M. Cyclophosphamide-induced alterations of bone marrow endothelium: implications in homing of marrow cells after transplantation. Exp Hematol. 1991;19:369–373
  13. Shirota T, Tavassoli M. Alterations of bone marrow sinus endothelium induced by ionizing irradiation: implications in the homing of intravenously transplanted marrow cells. Blood Cells. 1992;18:197–214
  14. Kopp HG, Avecilla ST, Hooper AT, et al. Tie2 activation contributes to hemangiogenic regeneration after myelosuppression. Blood. 2005;106:505–513
  15. Daldrup-Link HE, Link TM, Rummeny EJ, et al. Assessing permeability alterations of the blood-bone marrow barrier due to total body irradiation: in vivo quantification with contrast enhanced magnetic resonance imaging. Bone Marrow Transplant. 2000;25:71–78
  16. Slayton WB, Li XM, Butler J, et al. The role of the donor in the repair of the marrow vascular niche following hematopoietic stem cell transplant. Stem Cells. 2007;25:2945–2955
  17. Hadjantonakis AK, Gertsenstein M, Ikawa M, Okabe M, Nagy A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech Dev. 1998;76:79–90
  18. Brown MS, Basu SK, Falck JR, Ho YK, Goldstein JL. The scavenger cell pathway for lipoprotein degradation: specificity of the binding site that mediates the uptake of negatively-charged LDL by macrophages. J Supramol Struct. 1980;13:67–81
  19. Arbiser JL, Moses MA, Fernandez CA, et al. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc Natl Acad Sci U S A. 1997;94:861–866
  20. Zhang H, Wheeler KT. Radiation-induced DNA damage in tumors and normal tissues. I. Feasibility of estimating the hypoxic fraction. Radiat Res. 1993;136:77–88
  21. Fry RC, Begley TJ, Samson LD. Genome-wide responses to DNA-damaging agents. Annu Rev Microbiol. 2005;59:357–377
  22. Kruhlak MJ, Celeste A, Dellaire G, et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol. 2006;172:823–834
  23. Celeste A, Petersen S, Romanienko PJ, et al. Genomic instability in mice lacking histone H2AX. Science. 2002;296:922–927
  24. Norbury CJ, Zhivotovsky B. DNA damage-induced apoptosis. Oncogene. 2004;23:2797–2808
  25. Lowndes NF. DNA-damage signaling and apoptosis. Genome Biol. 2001;2:REPORTS4028.1 –4028.2
  26. Cande C, Cohen I, Daugas E, et al. Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie. 2002;84:215–222
  27. Susin SA, Daugas E, Ravagnan L, et al. Two distinct pathways leading to nuclear apoptosis. J Exp Med. 2000;192:571–580
  28. Zavitsanou K, Nguyen V, Greguric I, Chapman J, Ballantyne P, Katsifis A. Detection of apoptotic cell death in the thymus of dexamethasone treated rats using [(123)I]Annexin V and in situ oligonucleotide ligation. J Mol Histol. 2007;38:313–319
  29. Ansari B, Coates PJ, Greenstein BD, Hall PA. In situ end-labelling detects DNA strand breaks in apoptosis and other physiological and pathological states. J Pathol. 1993;170:1–8
  30. Eastman A, Barry MA. The origins of DNA breaks: a consequence of DNA damage, DNA repair, or apoptosis?. Cancer Invest. 1992;10:229–240
  31. Zuber P, Hamou MF, de Tribolet N. Identification of proliferating cells in human gliomas using the monoclonal antibody Ki-67. Neurosurgery. 1988;22:364–368
  32. Jalava P, Kuopio T, Juntti-Patinen L, Kotkansalo T, Kronqvist P, Collan Y. Ki67 immunohistochemistry: a valuable marker in prognostication but with a risk of misclassification: proliferation subgroups formed based on Ki67 immunoreactivity and standardized mitotic index. Histopathology. 2006;48:674–682
  33. Yamazaki K, Allen TD. Ultrastructural and morphometric alterations in bone marrow stromal tissue after 7 Gy irradiation. Blood Cells. 1991;17:527–549
  34. Paris F, Fuks Z, Kang A, et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293:293–297
  35. Fuks Z, Persaud RS, Alfieri A, et al. Basic fibroblast growth factor protects endothelial cells against radiation-induced programmed cell death in vitro and in vivo. Cancer Res. 1994;54:2582–2590
  36. Rubin P, Finkelstein J, Shapiro D. Molecular biology mechanisms in the radiation induction of pulmonary injury syndromes: interrelationship between the alveolar macrophage and the septal fibroblast. Int J Radiat Oncol Biol Phys. 1992;24:93–101
  37. Hopewell JW, Calvo W, Jaenke R, Reinhold HS, Robbins ME, Whitehouse EM. Microvasculature and radiation damage. Recent Results Cancer Res. 1993;130:1–16
  38. Garcia-Barros M, Paris F, Cordon-Cardo C, et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science. 2003;300:1155–1159
  39. Eissner G, Kohlhuber F, Grell M, et al. Critical involvement of transmembrane tumor necrosis factor-alpha in endothelial programmed cell death mediated by ionizing radiation and bacterial endotoxin. Blood. 1995;86:4184–4193
  40. Gaugler MH, Squiban C, Claraz M, et al. Characterization of the response of human bone marrow endothelial cells to in vitro irradiation. Br J Haematol. 1998;103:980–989
  41. Hadden CT. Repair and subsequent fragmentation of deoxyribonucleic acid in ultraviolet-irradiated Bacillus subtilis recA. J Bacteriol. 1977;132:856–861
  42. Pastukh V, Ruchko M, Gorodnya O, Wilson GL, Gillespie MN. Sequence-specific oxidative base modifications in hypoxia-inducible genes. Free Radic Biol Med. 2007;43:1616–1626
  43. Knospe WH, Blom J, Crosby WH. Regeneration of locally irradiated bone marrow. I. Dose dependent, long-term changes in the rat, with particular emphasis upon vascular and stromal reaction. Blood. 1966;28:398–415

PII: S0301-472X(08)00306-8

doi: 10.1016/j.exphem.2008.06.009

Experimental Hematology
Volume 36, Issue 9 , Pages 1143-1156.e3 , September 2008