Skip to main content
Top
Published in: Vascular Cell 1/2013

Open Access 01-12-2013 | Review

The effects of radiation on angiogenesis

Authors: Peter Grabham, Preety Sharma

Published in: Vascular Cell | Issue 1/2013

Login to get access

Abstract

The average human body contains tens of thousands of miles of vessels that permeate every tissue down to the microscopic level. This makes the human vasculature a prime target for an agent like radiation that originates from a source and passes through the body. Exposure to radiation released during nuclear accidents and explosions, or during cancer radiotherapy, is well known to cause vascular pathologies because of the ionizing effects of electromagnetic radiations (photons) such as gamma rays. There is however, another type of less well-known radiation – charged ion particles, and these atoms stripped of electrons, have different physical properties to the photons of electromagnetic radiation. They are either found in space or created on earth by particle collider facilities, and are of significant recent interest due to their enhanced effectiveness and increasing use in cancer radiotherapy, as well as a health risk to the growing number of people spending time in the space environment. Although there is to date, relatively few studies on the effects of charged particles on the vascular system, a very different picture of the biological effects of these particles compared to photons is beginning to emerge. These under researched biological effects of ion particles have a large impact on the health consequences of exposure. In this short review, we will discuss the effects of charged particles on an important biological process of the vascular system, angiogenesis, which creates and maintains the vasculature and is highly important in tumor vasculogenesis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Graebe A, Schuck EL, Lensing P, Putcha L, Derendorf H: Physiological, pharmacokinetic, and pharmacodynamic changes in space. J Clinical Pharmacol. 2004, 44: 837-853. 10.1177/0091270004267193.CrossRef Graebe A, Schuck EL, Lensing P, Putcha L, Derendorf H: Physiological, pharmacokinetic, and pharmacodynamic changes in space. J Clinical Pharmacol. 2004, 44: 837-853. 10.1177/0091270004267193.CrossRef
2.
go back to reference Jurado JA, Bashir R, Burket MW: Radiation-induced peripheral artery disease. Catheterization Cardiov Interv: Off J Soc Cardiac Angiogr Interv. 2008, 72: 563-568.CrossRef Jurado JA, Bashir R, Burket MW: Radiation-induced peripheral artery disease. Catheterization Cardiov Interv: Off J Soc Cardiac Angiogr Interv. 2008, 72: 563-568.CrossRef
3.
go back to reference Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, Hall P, et al: Systematic review and meta-analysis of circulatory disease from exposure to low-level ionizing radiation and estimates of potential population mortality risks. Environ Health Perspectives. 2012, 120: 1503-1511. 10.1289/ehp.1204982.CrossRef Little MP, Azizova TV, Bazyka D, Bouffler SD, Cardis E, Chekin S, Chumak VV, Cucinotta FA, de Vathaire F, Hall P, et al: Systematic review and meta-analysis of circulatory disease from exposure to low-level ionizing radiation and estimates of potential population mortality risks. Environ Health Perspectives. 2012, 120: 1503-1511. 10.1289/ehp.1204982.CrossRef
4.
go back to reference Preston DL, Shimizu Y, Pierce DA, Suyama A, Mabuchi K: Studies of mortality of atomic bomb survivors. Report 13: solid cancer and noncancer disease mortality: 1950–1997. Radiation Res. 2003, 160: 381-407. 10.1667/RR3049.CrossRefPubMed Preston DL, Shimizu Y, Pierce DA, Suyama A, Mabuchi K: Studies of mortality of atomic bomb survivors. Report 13: solid cancer and noncancer disease mortality: 1950–1997. Radiation Res. 2003, 160: 381-407. 10.1667/RR3049.CrossRefPubMed
6.
go back to reference Durante M, Loeffler JS: Charged particles in radiation oncology. Nat Rev Clinical Oncol. 2010, 7: 37-43. 10.1038/nrclinonc.2009.183.CrossRef Durante M, Loeffler JS: Charged particles in radiation oncology. Nat Rev Clinical Oncol. 2010, 7: 37-43. 10.1038/nrclinonc.2009.183.CrossRef
7.
go back to reference Jakel O: Medical physics aspects of particle therapy. Radiat Prot Dosimetry. 2009, 137: 156-166. 10.1093/rpd/ncp192.CrossRefPubMed Jakel O: Medical physics aspects of particle therapy. Radiat Prot Dosimetry. 2009, 137: 156-166. 10.1093/rpd/ncp192.CrossRefPubMed
8.
go back to reference Jones B: The case for particle therapy. British J Radiol. 2006, 79: 24-31. 10.1259/bjr/81790390.CrossRef Jones B: The case for particle therapy. British J Radiol. 2006, 79: 24-31. 10.1259/bjr/81790390.CrossRef
9.
go back to reference Jones B: The potential clinical advantages of charged particle radiotherapy using protons or light ions. Clinical Oncol. 2008, 20: 555-563. 10.1016/j.clon.2008.02.012.CrossRef Jones B: The potential clinical advantages of charged particle radiotherapy using protons or light ions. Clinical Oncol. 2008, 20: 555-563. 10.1016/j.clon.2008.02.012.CrossRef
10.
go back to reference Nelson GA: Fundamental space radiobiology. Gravitation Space Biol Bull: Publ Am Soc Gravitation Space Biol. 2003, 16: 29-36. Nelson GA: Fundamental space radiobiology. Gravitation Space Biol Bull: Publ Am Soc Gravitation Space Biol. 2003, 16: 29-36.
11.
go back to reference Schimmerling W, Cucinotta FA: Dose and dose rate effectiveness of space radiation. Radiation Prot Dosimetry. 2006, 122: 349-353.CrossRef Schimmerling W, Cucinotta FA: Dose and dose rate effectiveness of space radiation. Radiation Prot Dosimetry. 2006, 122: 349-353.CrossRef
12.
go back to reference Grabham P, Sharma P, Bigelow A, Geard C: Two distinct types of the inhibition of vasculogenesis by different species of charged particles. Vascular Cell. 2013, 5: 16-10.1186/2045-824X-5-16.PubMedCentralCrossRefPubMed Grabham P, Sharma P, Bigelow A, Geard C: Two distinct types of the inhibition of vasculogenesis by different species of charged particles. Vascular Cell. 2013, 5: 16-10.1186/2045-824X-5-16.PubMedCentralCrossRefPubMed
13.
go back to reference Goodhead DT: Energy deposition stochastics and track structure: what about the target?. Radiation Prot Dosimetry. 2006, 122: 3-15.CrossRef Goodhead DT: Energy deposition stochastics and track structure: what about the target?. Radiation Prot Dosimetry. 2006, 122: 3-15.CrossRef
14.
go back to reference Dicello JF: Absorption characteristics of protons and photons in tissue. Technol Cancer Res Treat. 2007, 6: 25-29.CrossRefPubMed Dicello JF: Absorption characteristics of protons and photons in tissue. Technol Cancer Res Treat. 2007, 6: 25-29.CrossRefPubMed
15.
go back to reference Liamsuwan T, Uehara S, Emfietzoglou D, Nikjoo H: Physical and biophysical properties of proton tracks of energies 1 keV to 300 MeV in water. Int J Radiation Biol. 2011, 87: 141-160. 10.3109/09553002.2010.518204.CrossRef Liamsuwan T, Uehara S, Emfietzoglou D, Nikjoo H: Physical and biophysical properties of proton tracks of energies 1 keV to 300 MeV in water. Int J Radiation Biol. 2011, 87: 141-160. 10.3109/09553002.2010.518204.CrossRef
16.
go back to reference Zeitlin C, Hassler DM, Cucinotta FA, Ehresmann B, Wimmer-Schweingruber RF, Brinza DE, Kang S, Weigle G, Bottcher S, Bohm E, et al: Measurements of energetic particle radiation in transit to mars on the mars science laboratory. Science. 2013, 340: 1080-1084. 10.1126/science.1235989.CrossRefPubMed Zeitlin C, Hassler DM, Cucinotta FA, Ehresmann B, Wimmer-Schweingruber RF, Brinza DE, Kang S, Weigle G, Bottcher S, Bohm E, et al: Measurements of energetic particle radiation in transit to mars on the mars science laboratory. Science. 2013, 340: 1080-1084. 10.1126/science.1235989.CrossRefPubMed
17.
go back to reference Cucinotta FA, Kim M-HY, Chappell LJ, Huff JL: How safe is safe enough? Radiation risk for a human mission to mars. PloS One. 2013, 8: e74988-10.1371/journal.pone.0074988.PubMedCentralCrossRefPubMed Cucinotta FA, Kim M-HY, Chappell LJ, Huff JL: How safe is safe enough? Radiation risk for a human mission to mars. PloS One. 2013, 8: e74988-10.1371/journal.pone.0074988.PubMedCentralCrossRefPubMed
18.
go back to reference Durante M, Kronenberg A: Ground-based research with heavy ions for space radiation protection. Adv Space Res: Off J Committee Space Res. 2005, 35: 180-184. 10.1016/j.asr.2004.12.034.CrossRef Durante M, Kronenberg A: Ground-based research with heavy ions for space radiation protection. Adv Space Res: Off J Committee Space Res. 2005, 35: 180-184. 10.1016/j.asr.2004.12.034.CrossRef
19.
go back to reference Held KD: Effects of low fluences of radiations found in space on cellular systems. Int J radiation Biol. 2009, 85: 379-390. 10.1080/09553000902838558.CrossRef Held KD: Effects of low fluences of radiations found in space on cellular systems. Int J radiation Biol. 2009, 85: 379-390. 10.1080/09553000902838558.CrossRef
20.
go back to reference Asaithamby A, Chen DJ: Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation. Mutation Res. 2011, 711: 87-99. 10.1016/j.mrfmmm.2010.11.002.PubMedCentralCrossRefPubMed Asaithamby A, Chen DJ: Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation. Mutation Res. 2011, 711: 87-99. 10.1016/j.mrfmmm.2010.11.002.PubMedCentralCrossRefPubMed
21.
go back to reference Blakely EA, Kronenberg A: Heavy-ion radiobiology: new approaches to delineate mechanisms underlying enhanced biological effectiveness. Radiation Res. 1998, 150: S126-S145. 10.2307/3579815.CrossRefPubMed Blakely EA, Kronenberg A: Heavy-ion radiobiology: new approaches to delineate mechanisms underlying enhanced biological effectiveness. Radiation Res. 1998, 150: S126-S145. 10.2307/3579815.CrossRefPubMed
22.
go back to reference Durante M, Cucinotta FA: Heavy ion carcinogenesis and human space exploration. Nature Rev Cancer. 2008, 8: 465-472. 10.1038/nrc2391.CrossRef Durante M, Cucinotta FA: Heavy ion carcinogenesis and human space exploration. Nature Rev Cancer. 2008, 8: 465-472. 10.1038/nrc2391.CrossRef
23.
go back to reference Prise KM, Pinto M, Newman HC, Michael BD: A review of studies of ionizing radiation-induced double-strand break clustering. Radiation Res. 2001, 156: 572-576. 10.1667/0033-7587(2001)156[0572:AROSOI]2.0.CO;2.CrossRefPubMed Prise KM, Pinto M, Newman HC, Michael BD: A review of studies of ionizing radiation-induced double-strand break clustering. Radiation Res. 2001, 156: 572-576. 10.1667/0033-7587(2001)156[0572:AROSOI]2.0.CO;2.CrossRefPubMed
24.
go back to reference Grabham P, Bigelow A, Geard C: DNA damage foci formation and decline in two-dimensional monolayers and in three-dimensional human vessel models: differential effects according to radiation quality. Int J Radiation Biol. 2012, 88: 493-500. 10.3109/09553002.2012.679382.CrossRef Grabham P, Bigelow A, Geard C: DNA damage foci formation and decline in two-dimensional monolayers and in three-dimensional human vessel models: differential effects according to radiation quality. Int J Radiation Biol. 2012, 88: 493-500. 10.3109/09553002.2012.679382.CrossRef
25.
go back to reference Grabham P, Hu B, Sharma P, Geard C: Effects of ionizing radiation on three-dimensional human vessel models: differential effects according to radiation quality and cellular development. Radiation Res. 2011, 175: 21-28. 10.1667/RR2289.1.CrossRefPubMed Grabham P, Hu B, Sharma P, Geard C: Effects of ionizing radiation on three-dimensional human vessel models: differential effects according to radiation quality and cellular development. Radiation Res. 2011, 175: 21-28. 10.1667/RR2289.1.CrossRefPubMed
26.
go back to reference Girdhani S, Sachs R, Hlatky L: Biological effects of proton radiation: what we know and don’t know. Radiation Res. 2013, 179: 257-272. 10.1667/RR2839.1.CrossRefPubMed Girdhani S, Sachs R, Hlatky L: Biological effects of proton radiation: what we know and don’t know. Radiation Res. 2013, 179: 257-272. 10.1667/RR2839.1.CrossRefPubMed
27.
go back to reference Moeller BJ, Cao Y, Li CY, Dewhirst MW: Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 2004, 5: 429-441. 10.1016/S1535-6108(04)00115-1.CrossRefPubMed Moeller BJ, Cao Y, Li CY, Dewhirst MW: Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 2004, 5: 429-441. 10.1016/S1535-6108(04)00115-1.CrossRefPubMed
28.
go back to reference Park CM, Park MJ, Kwak HJ, Lee HC, Kim MS, Lee SH, Park IC, Rhee CH, Hong SI: Ionizing radiation enhances matrix metalloproteinase-2 secretion and invasion of glioma cells through Src/epidermal growth factor receptor-mediated p38/Akt and phosphatidylinositol 3-kinase/Akt signaling pathways. Cancer Res. 2006, 66: 8511-8519. 10.1158/0008-5472.CAN-05-4340.CrossRefPubMed Park CM, Park MJ, Kwak HJ, Lee HC, Kim MS, Lee SH, Park IC, Rhee CH, Hong SI: Ionizing radiation enhances matrix metalloproteinase-2 secretion and invasion of glioma cells through Src/epidermal growth factor receptor-mediated p38/Akt and phosphatidylinositol 3-kinase/Akt signaling pathways. Cancer Res. 2006, 66: 8511-8519. 10.1158/0008-5472.CAN-05-4340.CrossRefPubMed
29.
go back to reference Sofia Vala I, Martins LR, Imaizumi N, Nunes RJ, Rino J, Kuonen F, Carvalho LM, Ruegg C, Grillo IM, Barata JT, et al: Low doses of ionizing radiation promote tumor growth and metastasis by enhancing angiogenesis. PloS One. 2010, 5: e11222-10.1371/journal.pone.0011222.PubMedCentralCrossRefPubMed Sofia Vala I, Martins LR, Imaizumi N, Nunes RJ, Rino J, Kuonen F, Carvalho LM, Ruegg C, Grillo IM, Barata JT, et al: Low doses of ionizing radiation promote tumor growth and metastasis by enhancing angiogenesis. PloS One. 2010, 5: e11222-10.1371/journal.pone.0011222.PubMedCentralCrossRefPubMed
30.
go back to reference Sonveaux P, Brouet A, Havaux X, Gregoire V, Dessy C, Balligand JL, Feron O: Irradiation-induced angiogenesis through the up-regulation of the nitric oxide pathway: implications for tumor radiotherapy. Cancer Res. 2003, 63: 1012-1019.PubMed Sonveaux P, Brouet A, Havaux X, Gregoire V, Dessy C, Balligand JL, Feron O: Irradiation-induced angiogenesis through the up-regulation of the nitric oxide pathway: implications for tumor radiotherapy. Cancer Res. 2003, 63: 1012-1019.PubMed
31.
go back to reference Gorski DH, Beckett MA, Jaskowiak NT, Calvin DP, Mauceri HJ, Salloum RM, Seetharam S, Koons A, Hari DM, Kufe DW, Weichselbaum RR: Blockage of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res. 1999, 59: 3374-3378.PubMed Gorski DH, Beckett MA, Jaskowiak NT, Calvin DP, Mauceri HJ, Salloum RM, Seetharam S, Koons A, Hari DM, Kufe DW, Weichselbaum RR: Blockage of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res. 1999, 59: 3374-3378.PubMed
32.
go back to reference Hlatky L, Tsionou C, Hahnfeldt P, Coleman CN: Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res. 1994, 54: 6083-6086.PubMed Hlatky L, Tsionou C, Hahnfeldt P, Coleman CN: Mammary fibroblasts may influence breast tumor angiogenesis via hypoxia-induced vascular endothelial growth factor up-regulation and protein expression. Cancer Res. 1994, 54: 6083-6086.PubMed
33.
go back to reference Girdhani S, Lamont C, Hahnfeldt P, Abdollahi A, Hlatky L: Proton irradiation suppresses angiogenic genes and impairs cell invasion and tumor growth. Radiation Res. 2012, 178: 33-45. 10.1667/RR2724.1.CrossRefPubMed Girdhani S, Lamont C, Hahnfeldt P, Abdollahi A, Hlatky L: Proton irradiation suppresses angiogenic genes and impairs cell invasion and tumor growth. Radiation Res. 2012, 178: 33-45. 10.1667/RR2724.1.CrossRefPubMed
34.
go back to reference Jang GH, Ha JH, Huh TL, Lee YM: Effect of proton beam on blood vessel formation in early developing zebrafish (Danio rerio) embryos. Archives Pharmacal Res. 2008, 31: 779-785. 10.1007/s12272-001-1226-1.CrossRef Jang GH, Ha JH, Huh TL, Lee YM: Effect of proton beam on blood vessel formation in early developing zebrafish (Danio rerio) embryos. Archives Pharmacal Res. 2008, 31: 779-785. 10.1007/s12272-001-1226-1.CrossRef
35.
go back to reference Boyd SR, Gittos A, Richter M, Hungerford JL, Errington RD, Cree IA: Proton beam therapy and iris neovascularisation in uveal melanoma. Eye. 2006, 20: 832-836. 10.1038/sj.eye.6702072.CrossRefPubMed Boyd SR, Gittos A, Richter M, Hungerford JL, Errington RD, Cree IA: Proton beam therapy and iris neovascularisation in uveal melanoma. Eye. 2006, 20: 832-836. 10.1038/sj.eye.6702072.CrossRefPubMed
36.
go back to reference Takahashi Y, Teshima T, Kawaguchi N, Hamada Y, Mori S, Madachi A, Ikeda S, Mizuno H, Ogata T, Nojima K, et al: Heavy ion irradiation inhibits in vitro angiogenesis even at sublethal dose. Cancer Res. 2003, 63: 4253-4257.PubMed Takahashi Y, Teshima T, Kawaguchi N, Hamada Y, Mori S, Madachi A, Ikeda S, Mizuno H, Ogata T, Nojima K, et al: Heavy ion irradiation inhibits in vitro angiogenesis even at sublethal dose. Cancer Res. 2003, 63: 4253-4257.PubMed
37.
go back to reference Mao XW, Favre CJ, Fike JR, Kubinova L, Anderson E, Campbell-Beachler M, Jones T, Smith A, Rightnar S, Nelson GA: High-LET radiation-induced response of microvessels in the hippocampus. Radiation Res. 2010, 173: 486-493. 10.1667/RR1728.1.CrossRefPubMed Mao XW, Favre CJ, Fike JR, Kubinova L, Anderson E, Campbell-Beachler M, Jones T, Smith A, Rightnar S, Nelson GA: High-LET radiation-induced response of microvessels in the hippocampus. Radiation Res. 2010, 173: 486-493. 10.1667/RR1728.1.CrossRefPubMed
Metadata
Title
The effects of radiation on angiogenesis
Authors
Peter Grabham
Preety Sharma
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Vascular Cell / Issue 1/2013
Electronic ISSN: 2045-824X
DOI
https://doi.org/10.1186/2045-824X-5-19

Other articles of this Issue 1/2013

Vascular Cell 1/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine