Tissue-sparing effect of x-ray microplanar beams particularly in the CNS: Is a bystander effect involved?

F. Avraham Dilmanian, Yun Qu, Ludwig E. Feinendegen, Louis A. Peña, Tigran Bacarian, Fritz A. Henn, John Kalef-Ezra, Su Liu, Zhong Zhong, John W. McDonald

Research output: Contribution to journalArticle

Abstract

Objective: Normal tissues, including the central nervous system, tolerate single exposures to narrow planes of synchrotron-generated x-rays (microplanar beams; microbeams) up to several hundred Gy. The repairs apparently involve the microvasculature and the glial system. We evaluate a hypothesis on the involvement of bystander effects in these repairs. Methods: Confluent cultures of bovine aortic endothelial cells were irradiated with three parallel 27-μm microbeams at 24 Gy. Rats' spinal cords were transaxially irradiated with a single microplanar beam, 270 μm thick, at 750 Gy; the dose distribution in tissue was calculated. Results: Within 6 hours following irradiation of the cell culture the hit cells died, apparently by apoptosis, were lost, and the confluency was maintained. The spinal cord study revealed a loss of oligodendrocytes, astrocytes, and myelin in 2 weeks, but by 3 months repopulation and remyelination was nearly complete. Monte Carlo simulations showed that the microbeam dose fell from the peak's 80% to 20% in 9 μm. Conclusions: In both studies the repair processes could have involved "beneficial" bystander effects leading to tissue restoration, most likely through the release of growth factors, such as cytokines, and the initiation of cell-signaling cascades. In cell culture these events could have promoted fast disappearance of the hit cells and fast structural response of the surviving neighboring cells, while in the spinal cord study similar events could have been promoting angiogenesis to replace damaged capillary blood vessels, and proliferation, migration, and differentiation of the progenitor glial cells to produce new, mature, and functional glial cells.

Original languageEnglish (US)
Pages (from-to)69-77
Number of pages9
JournalExperimental Hematology
Volume35
Issue number4 SUPPL.
DOIs
StatePublished - Apr 2007
Externally publishedYes

Fingerprint

Bystander Effect
X-Rays
Neuroglia
Spinal Cord
Cell Culture Techniques
Synchrotrons
Oligodendroglia
Tissue Distribution
Myelin Sheath
Microvessels
Astrocytes
Blood Vessels
Intercellular Signaling Peptides and Proteins
Stem Cells
Central Nervous System
Endothelial Cells
Apoptosis
Cytokines

ASJC Scopus subject areas

  • Cancer Research
  • Cell Biology
  • Genetics
  • Hematology
  • Oncology
  • Transplantation

Cite this

Dilmanian, F. A., Qu, Y., Feinendegen, L. E., Peña, L. A., Bacarian, T., Henn, F. A., ... McDonald, J. W. (2007). Tissue-sparing effect of x-ray microplanar beams particularly in the CNS: Is a bystander effect involved? Experimental Hematology, 35(4 SUPPL.), 69-77. https://doi.org/10.1016/j.exphem.2007.01.014

Tissue-sparing effect of x-ray microplanar beams particularly in the CNS : Is a bystander effect involved? / Dilmanian, F. Avraham; Qu, Yun; Feinendegen, Ludwig E.; Peña, Louis A.; Bacarian, Tigran; Henn, Fritz A.; Kalef-Ezra, John; Liu, Su; Zhong, Zhong; McDonald, John W.

In: Experimental Hematology, Vol. 35, No. 4 SUPPL., 04.2007, p. 69-77.

Research output: Contribution to journalArticle

Dilmanian, FA, Qu, Y, Feinendegen, LE, Peña, LA, Bacarian, T, Henn, FA, Kalef-Ezra, J, Liu, S, Zhong, Z & McDonald, JW 2007, 'Tissue-sparing effect of x-ray microplanar beams particularly in the CNS: Is a bystander effect involved?', Experimental Hematology, vol. 35, no. 4 SUPPL., pp. 69-77. https://doi.org/10.1016/j.exphem.2007.01.014
Dilmanian, F. Avraham ; Qu, Yun ; Feinendegen, Ludwig E. ; Peña, Louis A. ; Bacarian, Tigran ; Henn, Fritz A. ; Kalef-Ezra, John ; Liu, Su ; Zhong, Zhong ; McDonald, John W. / Tissue-sparing effect of x-ray microplanar beams particularly in the CNS : Is a bystander effect involved?. In: Experimental Hematology. 2007 ; Vol. 35, No. 4 SUPPL. pp. 69-77.
@article{9776455c11784ddfbc93f46d4c8daffa,
title = "Tissue-sparing effect of x-ray microplanar beams particularly in the CNS: Is a bystander effect involved?",
abstract = "Objective: Normal tissues, including the central nervous system, tolerate single exposures to narrow planes of synchrotron-generated x-rays (microplanar beams; microbeams) up to several hundred Gy. The repairs apparently involve the microvasculature and the glial system. We evaluate a hypothesis on the involvement of bystander effects in these repairs. Methods: Confluent cultures of bovine aortic endothelial cells were irradiated with three parallel 27-μm microbeams at 24 Gy. Rats' spinal cords were transaxially irradiated with a single microplanar beam, 270 μm thick, at 750 Gy; the dose distribution in tissue was calculated. Results: Within 6 hours following irradiation of the cell culture the hit cells died, apparently by apoptosis, were lost, and the confluency was maintained. The spinal cord study revealed a loss of oligodendrocytes, astrocytes, and myelin in 2 weeks, but by 3 months repopulation and remyelination was nearly complete. Monte Carlo simulations showed that the microbeam dose fell from the peak's 80{\%} to 20{\%} in 9 μm. Conclusions: In both studies the repair processes could have involved {"}beneficial{"} bystander effects leading to tissue restoration, most likely through the release of growth factors, such as cytokines, and the initiation of cell-signaling cascades. In cell culture these events could have promoted fast disappearance of the hit cells and fast structural response of the surviving neighboring cells, while in the spinal cord study similar events could have been promoting angiogenesis to replace damaged capillary blood vessels, and proliferation, migration, and differentiation of the progenitor glial cells to produce new, mature, and functional glial cells.",
author = "Dilmanian, {F. Avraham} and Yun Qu and Feinendegen, {Ludwig E.} and Pe{\~n}a, {Louis A.} and Tigran Bacarian and Henn, {Fritz A.} and John Kalef-Ezra and Su Liu and Zhong Zhong and McDonald, {John W.}",
year = "2007",
month = "4",
doi = "10.1016/j.exphem.2007.01.014",
language = "English (US)",
volume = "35",
pages = "69--77",
journal = "Experimental Hematology",
issn = "0301-472X",
publisher = "Elsevier Inc.",
number = "4 SUPPL.",

}

TY - JOUR

T1 - Tissue-sparing effect of x-ray microplanar beams particularly in the CNS

T2 - Is a bystander effect involved?

AU - Dilmanian, F. Avraham

AU - Qu, Yun

AU - Feinendegen, Ludwig E.

AU - Peña, Louis A.

AU - Bacarian, Tigran

AU - Henn, Fritz A.

AU - Kalef-Ezra, John

AU - Liu, Su

AU - Zhong, Zhong

AU - McDonald, John W.

PY - 2007/4

Y1 - 2007/4

N2 - Objective: Normal tissues, including the central nervous system, tolerate single exposures to narrow planes of synchrotron-generated x-rays (microplanar beams; microbeams) up to several hundred Gy. The repairs apparently involve the microvasculature and the glial system. We evaluate a hypothesis on the involvement of bystander effects in these repairs. Methods: Confluent cultures of bovine aortic endothelial cells were irradiated with three parallel 27-μm microbeams at 24 Gy. Rats' spinal cords were transaxially irradiated with a single microplanar beam, 270 μm thick, at 750 Gy; the dose distribution in tissue was calculated. Results: Within 6 hours following irradiation of the cell culture the hit cells died, apparently by apoptosis, were lost, and the confluency was maintained. The spinal cord study revealed a loss of oligodendrocytes, astrocytes, and myelin in 2 weeks, but by 3 months repopulation and remyelination was nearly complete. Monte Carlo simulations showed that the microbeam dose fell from the peak's 80% to 20% in 9 μm. Conclusions: In both studies the repair processes could have involved "beneficial" bystander effects leading to tissue restoration, most likely through the release of growth factors, such as cytokines, and the initiation of cell-signaling cascades. In cell culture these events could have promoted fast disappearance of the hit cells and fast structural response of the surviving neighboring cells, while in the spinal cord study similar events could have been promoting angiogenesis to replace damaged capillary blood vessels, and proliferation, migration, and differentiation of the progenitor glial cells to produce new, mature, and functional glial cells.

AB - Objective: Normal tissues, including the central nervous system, tolerate single exposures to narrow planes of synchrotron-generated x-rays (microplanar beams; microbeams) up to several hundred Gy. The repairs apparently involve the microvasculature and the glial system. We evaluate a hypothesis on the involvement of bystander effects in these repairs. Methods: Confluent cultures of bovine aortic endothelial cells were irradiated with three parallel 27-μm microbeams at 24 Gy. Rats' spinal cords were transaxially irradiated with a single microplanar beam, 270 μm thick, at 750 Gy; the dose distribution in tissue was calculated. Results: Within 6 hours following irradiation of the cell culture the hit cells died, apparently by apoptosis, were lost, and the confluency was maintained. The spinal cord study revealed a loss of oligodendrocytes, astrocytes, and myelin in 2 weeks, but by 3 months repopulation and remyelination was nearly complete. Monte Carlo simulations showed that the microbeam dose fell from the peak's 80% to 20% in 9 μm. Conclusions: In both studies the repair processes could have involved "beneficial" bystander effects leading to tissue restoration, most likely through the release of growth factors, such as cytokines, and the initiation of cell-signaling cascades. In cell culture these events could have promoted fast disappearance of the hit cells and fast structural response of the surviving neighboring cells, while in the spinal cord study similar events could have been promoting angiogenesis to replace damaged capillary blood vessels, and proliferation, migration, and differentiation of the progenitor glial cells to produce new, mature, and functional glial cells.

UR - http://www.scopus.com/inward/record.url?scp=33947260704&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33947260704&partnerID=8YFLogxK

U2 - 10.1016/j.exphem.2007.01.014

DO - 10.1016/j.exphem.2007.01.014

M3 - Article

C2 - 17379090

AN - SCOPUS:33947260704

VL - 35

SP - 69

EP - 77

JO - Experimental Hematology

JF - Experimental Hematology

SN - 0301-472X

IS - 4 SUPPL.

ER -