Skip to main content

Advertisement

SpringerLink
Log in

Bone marrow sinusoidal endothelium: damage and potential regeneration following cancer radiotherapy or chemotherapy

  • Review Paper
  • Published:
Angiogenesis Aims and scope Submit manuscript

Abstract

It is very well known that bone marrow (BM) microvasculature may possess a crucial role in the maintenance of homeostasis of BM due to mutual interactions between BM microvascular system and other physiological functions including haematopoiesis and osteogenesis. Chemotherapy and radiotherapy are known as main approaches for cancer treatment and also are known as the main cause of damage to the BM microvascular system. However, despite the importance of BM microvasculature in orchestrating various biological functions, less attention has been drawn to address the underlying mechanisms for the damage and to explore cellular and molecular mechanisms by which the recovery/regeneration of chemotherapy- and/or radiotherapy-induced BM microvascular system damage can occur. Therefore, in this review we firstly discuss the ultra-/structure and biological characteristics of BM microvascular system (sinusoids). Secondly, potential contribution of BM sinusoids is discussed in pathophysiological circumstances (bone remodelling, haematopoiesis, cancer bone metastasis, and haematological cancers). Thirdly, we address previous preclinical and clinical studies regarding chemotherapy- and irradiation-induced BM microvasculature damage. Finally, potential cellular and molecular mechanisms are discussed for the recovery/regeneration of damaged BM microvascular system, including the potential roles of endothelial progenitor cells, haematopoietic stem/progenitor cells, and stimulation of VEGF/VEGFR and Ang-1/Tie-2 signalling pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

BM:

Bone marrow

ECs:

Endothelial cell

BMSE:

Bone marrow sinusoidal endothelium

HSCs:

Haematopoietic stem cells

HCs:

Haematopoietic cells

MSCs:

Mesenchymal stem cells

SECs:

Sinusoidal endothelial cells

SDF-1:

Stromal cell-derived factor-1

VE-cadherin:

Vascular endothelial-cadherin

VEGF:

Vascular endothelial growth factor

VEGFR:

Vascular endothelial growth factor receptor

Sca 1:

Stem cell antigen 1

vWf:

von Willebrand factor

DiI-Ac-LDL:

DiI-acetylated-low density lipoprotein

EPCs:

Endothelial progenitor cells

AGE:

Advanced glycation end

IL:

Interleukin

GM-CSF:

Granulocyte macrophage colony-stimulating factor

TNF:

Tumour necrosis factor

G-CSF:

Granulocyte colony-stimulating factor

FGF:

Fibroblast growth factors

TGF:

Transforming growth factors

BMP:

Bone morphogenetic proteins

PDGF:

Platelet-derived growth factor

RER:

Rough endoplasmic reticulum

5-FU:

5-Fluorouracil

ALL:

Acute lymphoblastic leukaemia

CML:

Chronic myelogenous leukaemia

AML:

Acute myeloid leukaemia

MM:

Multiple myeloma

HSCT:

Haematopoietic stem cell transplantation

BMT:

Bone marrow transplantation

ELF4:

E74-like factor

CDK4:

Cyclin-dependent kinase-4

Ang-1:

Angiopoietin-1

References

  1. Saran U, Gemini Piperni S, Chatterjee S (2014) Role of angiogenesis in bone repair. Arch Biochem Biophys 561:109–117. doi:10.1016/j.abb.2014.07.006

    Article  CAS  PubMed  Google Scholar 

  2. Marenzana M, Arnett TR (2013) The key role of the blood supply to bone. Bone Res 1(3):203–215. doi:10.4248/BR201303001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rafii S, Butler JM, Ding BS (2016) Angiocrine functions of organ-specific endothelial cells. Nature 529(7586):316–325. doi:10.1038/nature17040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S (2009) Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 4(3):263–274. doi:10.1016/j.stem.2009.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kopp HG, Avecilla ST, Hooper AT, Shmelkov SV, Ramos CA, Zhang F, Rafii S (2005) Tie2 activation contributes to hemangiogenic regeneration after myelosuppression. Blood 106(2):505–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sapoznikov A, Pewzner-Jung Y, Kalchenko V, Krauthgamer R, Shachar I, Jung S (2008) Perivascular clusters of dendritic cells provide critical survival signals to B cells in bone marrow niches. Nat Immunol 9(4):388–395. doi:10.1038/ni1571

    Article  CAS  PubMed  Google Scholar 

  7. Kiel MJ, Morrison SJ (2006) Maintaining hematopoietic stem cells in the vascular niche. Immunity 25(6):862–864. doi:10.1016/j.immuni.2006.11.005

    Article  CAS  PubMed  Google Scholar 

  8. Kusumbe AP, Ramasamy SK, Itkin T, Mae MA, Langen UH, Betsholtz C, Lapidot T, Adams RH (2016) Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature 532(7599):380–384. doi:10.1038/nature17638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Marton PF (1975) Ultrastructural study of erythrophagocytosis in the rat bone marrow II. Iron metabolism in reticulum cells following red cell digestion. Scand J Haematol Suppl 23:27–48

    CAS  PubMed  Google Scholar 

  10. Shirota T, Tavassoli M (1991) Cyclophosphamide-induced alterations of bone marrow endothelium: implications in homing of marrow cells after transplantation. Exp Hematol 19(5):369–373

    CAS  PubMed  Google Scholar 

  11. Umezawa A, Harigaya K, Abe H, Watanabe Y (1990) Gap-junctional communication of bone marrow stromal cells is resistant to irradiation in vitro. Exp Hematol 18(9):1002–1007

    CAS  PubMed  Google Scholar 

  12. Wickramasinghe SN (1991) Observations on the ultrastructure of sinusoids and reticular cells in human bone marrow. Clin Lab Haematol 13(3):263–278

    Article  CAS  PubMed  Google Scholar 

  13. Irie S, Tavassoli M (1986) Structural features of isolated, fractionated bone marrow endothelium compared to sinus endothelium in situ. Scan Electron Microsc 2:615–619

    Google Scholar 

  14. Tavassoli M (1981) Structure and function of sinusoidal endothelium of bone marrow. Prog Clin Biol Res 59B:249–256

    CAS  PubMed  Google Scholar 

  15. Palade GE (1982) The vascular endothelium: problems for today and perspectives for tomorrow. Ann NY Acad Sci 401:265–272

    Article  CAS  PubMed  Google Scholar 

  16. Shaklai M, Tavassoli M (1978) Endothelial cell membrane: differences in the density of intramembranous particles between tissue- and blood-fronts revealed by freeze-fracture. Am J Anat 151(1):139–144. doi:10.1002/aja.1001510112

    Article  CAS  PubMed  Google Scholar 

  17. Li XM, Hu Z, Jorgenson ML, Slayton WB (2009) High levels of acetylated low-density lipoprotein uptake and low tyrosine kinase with immunoglobulin and epidermal growth factor homology domains-2 (Tie2) promoter activity distinguish sinusoids from other vessel types in murine bone marrow. Circulation 120(19):1910–1918. doi:10.1161/CIRCULATIONAHA.109.871574

    Article  CAS  PubMed  Google Scholar 

  18. Pusztaszeri MP, Seelentag W, Bosman FT (2006) Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J Histochem Cytochem 54(4):385–395. doi:10.1369/jhc.4A6514.2005

    Article  CAS  PubMed  Google Scholar 

  19. Harb R, Xie G, Lutzko C, Guo Y, Wang X, Hill CK, Kanel GC, DeLeve LD (2009) Bone marrow progenitor cells repair rat hepatic sinusoidal endothelial cells after liver injury. Gastroenterology 137(2):704–712. doi:10.1053/j.gastro.2009.05.009

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bailey AS, Willenbring H, Jiang S, Anderson DA, Schroeder DA, Wong MH, Grompe M, Fleming WH (2006) Myeloid lineage progenitors give rise to vascular endothelium. Proc Natl Acad Sci USA 103(35):13156–13161. doi:10.1073/pnas.0604203103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Geoffroy JS, Becker RP (1984) Endocytosis by endothelial phagocytes: uptake of bovine serum albumin-gold conjugates in bone marrow. J Ultrastruct Res 89(3):223–239

    Article  CAS  PubMed  Google Scholar 

  22. Qian H, Johansson S, McCourt P, Smedsrød B, Ekblom M, Johansson S (2009) Stabilins are expressed in bone marrow sinusoidal endothelial cells and mediate scavenging and cell adhesive functions. Biochem Biophys Res Commun 390(3):883–886. doi:10.1016/j.bbrc.2009.10.068

    Article  CAS  PubMed  Google Scholar 

  23. McCourt PA, Oteiza A, Cao B, Nilsson SK (2015) Isolation of murine bone marrow scavenging sinusoidal endothelial cells. Methods Mol Biol 1235:59–71. doi:10.1007/978-1-4939-1785-3_6

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. Brandi ML, Collin-Osdoby P (2006) Vascular biology and the skeleton. J Bone Miner Res 21(2):183–192. doi:10.1359/JBMR.050917

    Article  CAS  PubMed  Google Scholar 

  26. Chim SM, Tickner J, Chow ST, Kuek V, Guo B, Zhang G, Rosen V, Erber W, Xu J (2013) Angiogenic factors in bone local environment. Cytokine Growth Factor Rev 24(3):297–310. doi:10.1016/j.cytogfr.2013.03.008

    Article  CAS  PubMed  Google Scholar 

  27. Du X, Xie Y, Xian CJ, Chen L (2012) Role of FGFs/FGFRs in skeletal development and bone regeneration. J Cell Physiol 227(12):3731–3743. doi:10.1002/jcp.24083

    Article  CAS  PubMed  Google Scholar 

  28. Itkin T, Gur-Cohen S, Spencer JA, Schajnovitz A, Ramasamy SK, Kusumbe AP, Ledergor G, Jung Y, Milo I, Poulos MG, Kalinkovich A, Ludin A, Golan K, Khatib E, Kumari A, Kollet O, Shakhar G, Butler JM, Rafii S, Adams RH, Scadden DT, Lin CP, Lapidot T (2016) Corrigendum: Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature 538(7624):274. doi:10.1038/nature19088

    Article  CAS  PubMed  Google Scholar 

  29. Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH (1998) Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 188(3):465–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Furze RC, Rankin SM (2008) Neutrophil mobilization and clearance in the bone marrow. Immunology 125(3):281–288. doi:10.1111/j.1365-2567.2008.02950.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Mastro AM, Gay CV, Welch DR (2003) The skeleton as a unique environment for breast cancer cells. Clin Exp Metas 20(3):275–284

    Article  CAS  Google Scholar 

  32. Orr FW, Wang HH, Lafrenie RM, Scherbarth S, Nance DM (2000) Interactions between cancer cells and the endothelium in metastasis. J Pathol 190(3):310–329. doi:10.1002/(SICI)1096-9896(200002)190:3<310:AID-PATH525>3.0.CO;2-P

    Article  CAS  PubMed  Google Scholar 

  33. Thobe MN, Clark RJ, Bainer RO, Prasad SM, Rinker-Schaeffer CW (2011) From prostate to bone: key players in prostate cancer bone metastasis. Cancers 3(1):478–493. doi:10.3390/cancers3010478

    Article  PubMed  PubMed Central  Google Scholar 

  34. Welch DR, Harms JF, Mastro AM, Gay CV, Donahue HJ (2003) Breast cancer metastasis to bone: evolving models and research challenges. J Musculoskelet Neuronal Interact 3(1):30–38

    CAS  PubMed  Google Scholar 

  35. Lundstrom A, Holmbom J, Lindqvist C, Nordstrom T (1998) The role of alpha2 beta1 and alpha3 beta1 integrin receptors in the initial anchoring of MDA-MB-231 human breast cancer cells to cortical bone matrix. Biochem Biophys Res Commun 250(3):735–740. doi:10.1006/bbrc.1998.9389

    Article  CAS  PubMed  Google Scholar 

  36. Lehr JE, Pienta KJ (1998) Preferential adhesion of prostate cancer cells to a human bone marrow endothelial cell line. J Natl Cancer Inst 90(2):118–123

    Article  CAS  PubMed  Google Scholar 

  37. Taichman RS, Loberg RD, Mehra R, Pienta KJ (2007) The evolving biology and treatment of prostate cancer. J Clin Investig 117(9):2351–2361. doi:10.1172/JCI31791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Fajardo LF, Berthrong M (1988) Vascular lesions following radiation. Pathol Annu 23(Pt 1):297–330

    PubMed  Google Scholar 

  39. Russell NS, Hoving S, Heeneman S, Hage JJ, Woerdeman LAE, de Bree R, Lohuis PJFM, Smeele L, Cleutjens J, Valenkamp A, Dorresteijn LDA, Dalesio O, Daemen MJ, Stewart FA (2009) Novel insights into pathological changes in muscular arteries of radiotherapy patients. Radiother Oncol 92(3):477–483. doi:10.1016/j.radonc.2009.05.021

    Article  CAS  PubMed  Google Scholar 

  40. Weintraub NL, Jones WK, Manka D (2010) Understanding radiation-induced vascular disease. J Am Coll Cardiol 55(12):1237–1239. doi:10.1016/j.jacc.2009.11.053

    Article  CAS  PubMed  Google Scholar 

  41. Sharma P, Templin T, Grabham P (2013) Short term effects of gamma radiation on endothelial barrier function: uncoupling of PECAM-1. Microvasc Res 86:11–20. doi:10.1016/j.mvr.2012.11.007

    Article  CAS  PubMed  Google Scholar 

  42. Gianicolo ME, Gianicolo EA, Tramacere F, Andreassi MG, Portaluri M (2010) Effects of external irradiation of the neck region on intima media thickness of the common carotid artery. Cardiovasc Ultrasound 8:8. doi:10.1186/1476-7120-8-8

    Article  PubMed  PubMed Central  Google Scholar 

  43. Dorresteijn LD, Kappelle AC, Scholz NM, Munneke M, Scholma JT, Balm AJ, Bartelink H, Boogerd W (2005) Increased carotid wall thickening after radiotherapy on the neck. Eur J Cancer 41(7):1026–1030. doi:10.1016/j.ejca.2005.01.020

    Article  PubMed  Google Scholar 

  44. Atkinson S, Li YQ, Wong CS (2003) Changes in oligodendrocytes and myelin gene expression after radiation in the rodent spinal cord. Int J Radiat Oncol Biol Phys 57(4):1093–1100

    Article  CAS  PubMed  Google Scholar 

  45. Brenn T, Fletcher CD (2005) Radiation-associated cutaneous atypical vascular lesions and angiosarcoma: clinicopathologic analysis of 42 cases. Am J Surg Pathol 29(8):983–996

    PubMed  Google Scholar 

  46. Schultz-Hector S, Trott KR (2007) Radiation-induced cardiovascular diseases: is the epidemiologic evidence compatible with the radiobiologic data? Int J Radiat Oncol 67(1):10–18. doi:10.1016/j.ijrobp.2006.08.071

    Article  CAS  Google Scholar 

  47. Sievert W, Trott KR, Azimzadeh O, Tapio S, Zitzelsberger H, Multhoff G (2015) Late proliferating and inflammatory effects on murine microvascular heart and lung endothelial cells after irradiation. Radiother Oncol 117(2):376–381. doi:10.1016/j.radonc.2015.07.029

    Article  PubMed  Google Scholar 

  48. Narayan K, Cliff WJ (1982) Morphology of irradiated microvasculature: a combined in vivo and electron-microscopic study. Am J Pathol 106(1):47–62

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Slayton WB, Li XM, Butler J, Guthrie SM, Jorgensen ML, Wingard JR, Scott EW (2007) The role of the donor in the repair of the marrow vascular niche following hematopoietic stem cell transplant. Stem Cells 25(11):2945–2955

    Article  PubMed  Google Scholar 

  50. Fliedner TM, Graessle D, Paulsen C, Reimers K (2002) Structure and function of bone marrow hemopoiesis: mechanisms of response to ionizing radiation exposure. Cancer Biother Radiopharm 17(4):405–426. doi:10.1089/108497802760363204

    Article  CAS  PubMed  Google Scholar 

  51. Li XM, Hu Z, Jorgenson ML, Wingard JR, Slayton WB (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. Exp Hematol 36(9):1143–1156. doi:10.1016/j.exphem.2008.06.009

    Article  CAS  PubMed  Google Scholar 

  52. Shirota T, Tavassoli M (1992) Alterations of bone marrow sinus endothelium induced by ionizing irradiation: implications in the homing of intravenously transplanted marrow cells. Blood Cells 18(2):197–214

    CAS  PubMed  Google Scholar 

  53. Narayan K, Juneja S, Garcia C (1994) Effects of 5-fluorouracil or total-body irradiation on murine bone marrow microvasculature. Exp Hematol 22(2):142–148

    CAS  PubMed  Google Scholar 

  54. Noren-Nystrom U, Heyman M, Frisk P, Golovleva I, Sundstrom C, Porwit A, Roos G, Bergh A, Forestier E (2009) Vascular density in childhood acute lymphoblastic leukaemia correlates to biological factors and outcome. Br J Haematol 146(5):521–530. doi:10.1111/j.1365-2141.2009.07796.x

    Article  PubMed  Google Scholar 

  55. Aguayo A, Kantarjian H, Manshouri T, Gidel C, Estey E, Thomas D, Koller C, Estrov Z, O’Brien S, Keating M, Freireich E, Albitar M (2000) Angiogenesis in acute and chronic leukemias and myelodysplastic syndromes. Blood 96(6):2240–2245

    CAS  PubMed  Google Scholar 

  56. Hatfield KJ, Evensen L, Reikvam H, Lorens JB, Bruserud O (2012) Soluble mediators released by acute myeloid leukemia cells increase capillary-like networks. Eur J Haematol 89(6):478–490. doi:10.1111/ejh.12016

    Article  CAS  PubMed  Google Scholar 

  57. Alexandrakis MG, Pappa CA, Kokonozaki M, Boula A, Vyzoukaki R, Staphylaki D, Papadopoulou A, Androulakis N, Tsirakis G, Sfiridaki A (2015) Circulating serum levels of IL-20 in multiple myeloma patients: its significance in angiogenesis and disease activity. Med Oncol 32(3):42. doi:10.1007/s12032-015-0488-z

    Article  CAS  PubMed  Google Scholar 

  58. Negaard HF, Iversen N, Bowitz-Lothe IM, Sandset PM, Steinsvik B, Ostenstad B, Iversen PO (2009) Increased bone marrow microvascular density in haematological malignancies is associated with differential regulation of angiogenic factors. Leukemia 23(1):162–169. doi:10.1038/leu.2008.255

    Article  CAS  PubMed  Google Scholar 

  59. Schaefer C, Krause M, Fuhrhop I, Schroeder M, Algenstaedt P, Fiedler W, Ruther W, Hansen-Algenstaedt N (2008) Time-course-dependent microvascular alterations in a model of myeloid leukemia in vivo. Leukemia 22(1):59–65. doi:10.1038/sj.leu.2404947

    Article  CAS  PubMed  Google Scholar 

  60. Wellbrock J, Fiedler W (2011) Clinical experience with antiangiogenic therapy in leukemia. Curr Cancer Drug Targets 11(9):1053–1068

    Article  CAS  PubMed  Google Scholar 

  61. Cogle CR, Bosse RC, Brewer T, Migdady Y, Shirzad R, Kampen KR, Saki N (2015) Acute myeloid leukemia in the vascular niche. Cancer Lett. doi:10.1016/j.canlet.2015.05.007

    PubMed  Google Scholar 

  62. Xu Z, Zhang S, Zhou Q, Wang Y, Xia R (2014) Endocan, a potential prognostic and diagnostic biomarker of acute leukemia. Mol Cell Biochem 395(1–2):117–123. doi:10.1007/s11010-014-2117-0

    Article  CAS  PubMed  Google Scholar 

  63. Eissner G, Multhoff G, Holler E (1998) Influence of bacterial endotoxin on the allogenicity of human endothelial cells. Bone Marrow Transpl 21(12):1286–1288. doi:10.1038/sj.bmt.1701264

    Article  CAS  Google Scholar 

  64. Yamazaki K, Allen TD (1991) Ultrastructural and morphometric alterations in bone marrow stromal tissue after 7 Gy irradiation. Blood Cells 17(3):527–549

    CAS  PubMed  Google Scholar 

  65. Szumilas P, Barcew K, Baskiewicz-Masiuk M, Wiszniewska B, Ratajczak MZ, Machalinski B (2005) Effect of stem cell mobilization with cyclophosphamide plus granulocyte colony-stimulating factor on morphology of haematopoietic organs in mice. Cell Prolif 38(1):47–61. doi:10.1111/j.1365-2184.2005.00329.x

    Article  CAS  PubMed  Google Scholar 

  66. Carreras E, Diaz-Ricart M (2011) The role of the endothelium in the short-term complications of hematopoietic SCT. Bone Marrow Transpl 46(12):1495–1502. doi:10.1038/bmt.2011.65

    Article  CAS  Google Scholar 

  67. Cao X, Wu X, Frassica D, Yu B, Pang L, Xian L, Wan M, Lei W, Armour M, Tryggestad E, Wong J, Wen CY, Lu WW, Frassica FJ (2011) Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells. Proc Natl Acad Sci USA 108(4):1609–1614. doi:10.1073/pnas.1015350108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Salat C, Holler E, Kolb HJ, Pihusch R, Reinhardt B, Hiller E (1997) Endothelial cell markers in bone marrow transplant recipients with and without acute graft-versus-host disease. Bone Marrow Transpl 19(9):909–914. doi:10.1038/sj.bmt.1700767

    Article  CAS  Google Scholar 

  69. Wittels B (1980) Bone marrow biopsy changes following chemotherapy for acute leukemia. Am J Surg Pathol 4(2):135–142

    Article  CAS  PubMed  Google Scholar 

  70. Islam A (1987) Pattern of bone marrow regeneration following chemotherapy for acute myeloid leukemia. J Med 18(2):108–122

    CAS  PubMed  Google Scholar 

  71. Soligo DA, Lambertenghi Deliliers G, Servida F, Quirici N, Campiglio S, Tagliaferri E, Oriani A, Romitti L, Della Volpe A, Annaloro C (1998) Haematopoietic abnormalities after autologous stem cell transplantation in lymphoma patients. Bone Marrow Transpl 21(1):15–22. doi:10.1038/sj.bmt.1701053

    Article  CAS  Google Scholar 

  72. Schmid C, Isaacson PG (1992) Bone marrow trephine biopsy in lymphoproliferative disease. J Clin Pathol 45(9):745–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Brody JP, Krause JR, Penchansky L (1985) Bone marrow response to chemotherapy in acute lymphocytic leukaemia and acute non-lymphocytic leukaemia. Scand J Haematol 35(2):240–245

    Article  CAS  PubMed  Google Scholar 

  74. Nguyen TV, Melville A, Nath S, Story C, Howell S, Sutton R, Zannettino A, Revesz T (2015) Bone marrow recovery by morphometry during induction chemotherapy for acute lymphoblastic leukemia in children. PLoS ONE 10(5):e0126233. doi:10.1371/journal.pone.0126233

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Hurwitz N (1997) Bone marrow trephine biopsy changes following chemotherapy and/or bone marrow transplantation. Curr Diagn Pathol 4(4):196–202. doi:10.1016/S0968-6053(05)80062-6

    Article  Google Scholar 

  76. Li KD, Salama ME (2016) Therapy effect: impact on bone marrow morphology. Surg Pathol Clin 9(1):177–187. doi:10.1016/j.path.2015.09.006

    Article  CAS  PubMed  Google Scholar 

  77. Daldrup-Link HE, Henning T, Link TM (2007) MR imaging of therapy-induced changes of bone marrow. Eur Radiol 17(3):743–761. doi:10.1007/s00330-006-0404-1

    Article  PubMed  Google Scholar 

  78. Sivina M, Yamada T, Park CS, Puppi M, Coskun S, Hirschi K, Lacorazza HD (2011) The transcription factor E74-like factor controls quiescence of endothelial cells and their resistance to myeloablative treatments in bone marrow. Arterioscler Thromb Vasc Biol 31(5):1185–1191. doi:10.1161/atvbaha.111.224436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Johnson SM, Torrice CD, Bell JF, Monahan KB, Jiang Q, Wang Y, Ramsey MR, Jin J, Wong KK, Su L, Zhou D, Sharpless NE (2010) Mitigation of hematologic radiation toxicity in mice through pharmacological quiescence induced by CDK4/6 inhibition. J Clin Investig 120(7):2528–2536. doi:10.1172/JCI41402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Knospe WH, Blom J, Crosby WH (1966) Regeneration of locally irradiated bone marrow. I. Dose dependent, long-term changes in the rat, with particular emphasis upon vascular and stromal reaction. Blood 28(3):398–415

    CAS  PubMed  Google Scholar 

  81. Salter AB, Meadows SK, Muramoto GG, Himburg H, Doan P, Daher P, Russell L, Chen B, Chao NJ, Chute JP (2009) Endothelial progenitor cell infusion induces hematopoietic stem cell reconstitution in vivo. Blood 113(9):2104–2107. doi:10.1182/blood-2008-06-162941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85(3):221–228

    Article  CAS  PubMed  Google Scholar 

  83. Kvasnicka HM, Wickenhauser C, Thiele J, Varus E, Hamm K, Beelen DW, Schaefer UW (2003) Mixed chimerism of bone marrow vessels (endothelial cells, myofibroblasts) following allogeneic transplantation for chronic myelogenous leukemia. Leuk Lymphoma 44(2):321–328. doi:10.1080/1042819021000035699

    Article  PubMed  Google Scholar 

  84. Yan Z, Zeng L, Li Z, Zhang H, Chen W, Jia L, Chen C, Cheng H, Cao J, Xu K (2013) Bone marrow-derived endothelial progenitor cells promote hematopoietic reconstitution after hematopoietic stem cell transplantation. Transpl Proc 45(1):427–433

    Article  CAS  Google Scholar 

  85. Lee SP, Youn SW, Cho HJ, Li L, Kim TY, Yook HS, Chung JW, Hur J, Yoon CH, Park KW, Oh BH, Park YB, Kim HS (2006) Integrin-linked kinase, a hypoxia-responsive molecule, controls postnatal vasculogenesis by recruitment of endothelial progenitor cells to ischemic tissue. Circulation 114(2):150–159. doi:10.1161/CIRCULATIONAHA.105.595918

    Article  CAS  PubMed  Google Scholar 

  86. Carmona G, Chavakis E, Koehl U, Zeiher AM, Dimmeler S (2008) Activation of Epac stimulates integrin-dependent homing of progenitor cells. Blood 111(5):2640–2646. doi:10.1182/blood-2007-04-086231

    Article  CAS  PubMed  Google Scholar 

  87. Walter DH, Haendeler J, Reinhold J, Rochwalsky U, Seeger F, Honold J, Hoffmann J, Urbich C, Lehmann R, Arenzana-Seisdesdos F, Aicher A, Heeschen C, Fichtlscherer S, Zeiher AM, Dimmeler S (2005) Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease. Circ Res 97(11):1142–1151. doi:10.1161/01.RES.0000193596.94936.2c

    Article  CAS  PubMed  Google Scholar 

  88. Shaw TJ, Martin P (2009) Wound repair at a glance. J Cell Sci 122(Pt 18):3209–3213. doi:10.1242/jcs.031187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Smith DR, Polverini PJ, Kunkel SL, Orringer MB, Whyte RI, Burdick MD, Wilke CA, Strieter RM (1994) Inhibition of interleukin 8 attenuates angiogenesis in bronchogenic carcinoma. J Exp Med 179(5):1409–1415

    Article  CAS  PubMed  Google Scholar 

  90. Colotta F, Bussolino F, Polentarutti N, Guglielmetti A, Sironi M, Bocchietto E, De Rossi M, Mantovani A (1993) Differential expression of the common beta and specific alpha chains of the receptors for GM-CSF, IL-3, and IL-5 in endothelial cells. Exp Cell Res 206(2):311–317. doi:10.1006/excr.1993.1151

    Article  CAS  PubMed  Google Scholar 

  91. Toi M, Harris AL, Bicknell R (1991) Interleukin-4 is a potent mitogen for capillary endothelium. Biochem Biophys Res Commun 174(3):1287–1293

    Article  CAS  PubMed  Google Scholar 

  92. Giraudo E, Arese M, Toniatti C, Strasly M, Primo L, Mantovani A, Ciliberto G, Bussolini F (1996) IL-6 is an in vitro and in vivo autocrine growth factor for middle T antigen-transformed endothelial cells. J Immunol 157(6):2618–2623

    CAS  PubMed  Google Scholar 

  93. Bussolino F, Wang JM, Defilippi P, Turrini F, Sanavio F, Edgell CJ, Aglietta M, Arese P, Mantovani A (1989) Granulocyte- and granulocyte-macrophage-colony stimulating factors induce human endothelial cells to migrate and proliferate. Nature 337(6206):471–473. doi:10.1038/337471a0

    Article  CAS  PubMed  Google Scholar 

  94. Ribatti D, Presta M, Vacca A, Ria R, Giuliani R, Dell’Era P, Nico B, Roncali L, Dammacco F (1999) Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood 93(8):2627–2636

    CAS  PubMed  Google Scholar 

  95. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M (2002) MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2(4):289–300

    Article  CAS  PubMed  Google Scholar 

  96. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, Chimenti S, Landsman L, Abramovitch R, Keshet E (2006) VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124(1):175–189. doi:10.1016/j.cell.2005.10.036

    Article  CAS  PubMed  Google Scholar 

  97. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9(6):653–660. doi:10.1038/nm0603-653

    Article  CAS  PubMed  Google Scholar 

  98. Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, Kluge K, Schafer B, Hossfeld DK, Fiedler W (2000) In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95(10):3106–3112

    CAS  PubMed  Google Scholar 

  99. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95(4):343–353. doi:10.1161/01.RES.0000137877.89448.78

    Article  CAS  PubMed  Google Scholar 

  100. Bikfalvi A, Han ZC (1994) Angiogenic factors are hematopoietic growth factors and vice versa. Leukemia 8(3):523–529

    CAS  PubMed  Google Scholar 

  101. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA (2001) Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Investig 107(11):1395–1402. doi:10.1172/JCI12150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Schlaeppi JM, Gutzwiller S, Finkenzeller G, Fournier B (1997) 1,25-Dihydroxyvitamin D3 induces the expression of vascular endothelial growth factor in osteoblastic cells. Endocr Res 23(3):213–229

    Article  CAS  PubMed  Google Scholar 

  103. Juffer P, Jaspers RT, Lips P, Bakker AD, Klein-Nulend J (2012) Expression of muscle anabolic and metabolic factors in mechanically loaded MLO-Y4 osteocytes. Am J Physiol Endocrinol Metab 302(4):E389–E395. doi:10.1152/ajpendo.00320.2011

    Article  CAS  PubMed  Google Scholar 

  104. Trebec-Reynolds DP, Voronov I, Heersche JN, Manolson MF (2010) VEGF-A expression in osteoclasts is regulated by NF-kappaB induction of HIF-1alpha. J Cell Biochem 110(2):343–351. doi:10.1002/jcb.22542

    CAS  PubMed  Google Scholar 

  105. Mohle R, Green D, Moore MA, Nachman RL, Rafii S (1997) Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci USA 94(2):663–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131(2):324–336. doi:10.1016/j.cell.2007.08.025

    Article  CAS  PubMed  Google Scholar 

  107. Zhou B, Tsaknakis G, Coldwell KE, Khoo CP, Roubelakis MG, Chang CH, Pepperell E, Watt SM (2012) A novel function for the haemopoietic supportive murine bone marrow MS-5 mesenchymal stromal cell line in promoting human vasculogenesis and angiogenesis. Br J Haematol 157(3):299–311. doi:10.1111/j.1365-2141.2012.09050.x

    Article  CAS  PubMed  Google Scholar 

  108. Liem NL, Papa RA, Milross CG, Schmid MA, Tajbakhsh M, Choi S, Ramirez CD, Rice AM, Haber M, Norris MD, MacKenzie KL, Lock RB (2004) Characterization of childhood acute lymphoblastic leukemia xenograft models for the preclinical evaluation of new therapies. Blood 103(10):3905–3914. doi:10.1182/blood-2003-08-2911

    Article  CAS  PubMed  Google Scholar 

  109. Cui H, Li T, Wang L, Su Y, Xian CJ (2016) Dioscorea bulbifera polysaccharide and cyclophosphamide combination enhances anti-cervical cancer effect and attenuates immunosuppression and oxidative stress in mice. Sci Rep 5:19185. doi:10.1038/srep19185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Chiaming Fan (University of South Australia) for valuable discussion and thank Dr. Davood Mehrabani and Stem Cell and Transgenic Technology Research Center (Shiraz University of Medical Sciences) for their kind support. Authors’ own work discussed here was supported in part by National Health and Medical Research Council Australia (NHMRC) (0508046, 1010752) and Channel-7 Children Research Foundation of South Australia (13720, 161173, 171494). MH is supported by Research Training Program international (RTPi), President’s Scholarship of University of South Australia, and CJX is supported by NHMRC Senior Research Fellowship (0508047, 1042105). The funding sources had no roles in the writing of this review article.

Authors’ contribution

MH has reviewed the literature, written, and edited the manuscript. AH, SK, and YS have reviewed the literature, written and provided to the first and corresponding authors. CX played a significant role in the design, writing, and editing of this review article. All authors read and approved the final manuscript.

Availability of data and material

Please contact the corresponding author.

Author information

Authors and Affiliations

  1. Sansom Institute for Health Research, School of Pharmacy and Medical Sciences, University of South Australia, GPO Box 2471, Adelaide, SA, 5001, Australia

    Mohammadhossein Hassanshahi, Yu-Wen Su & Cory J. Xian

  2. Stem Cell and Transgenic Technology Research Centre, Shiraz University of Medical Sciences, Shiraz, Iran

    Alireza Hassanshahi

  3. PACE, University of Queensland School of Pharmacy, Woollloongabba, QLD, 4102, Australia

    Samira Khabbazi

Authors
  1. Mohammadhossein Hassanshahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alireza Hassanshahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samira Khabbazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu-Wen Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cory J. Xian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cory J. Xian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassanshahi, M., Hassanshahi, A., Khabbazi, S. et al. Bone marrow sinusoidal endothelium: damage and potential regeneration following cancer radiotherapy or chemotherapy. Angiogenesis 20, 427–442 (2017). https://doi.org/10.1007/s10456-017-9577-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10456-017-9577-2

Keywords

Search

Navigation