Beyond foreign-body-induced carcinogenesis: impact of reactive oxygen species derived from inflammatory cells in tumorigenic conversion and tumor progression

Our plain-English summary of Beyond foreign-body-induced carcinogenesis: impact of reactive oxygen species derived from inflammatory cells in tumorigenic conversion and tumor progression, by F. Okada (International Journal of Cancer, 2007).

The study

• Author: F. Okada
• Journal: International Journal of Cancer
• Published: 2007;121(11):2364-72
• Type of article: Review
• Cited by: 60 articles, as counted by NIH iCite
• Read it: PubMed · Publisher

Abstract

Foreign-body-induced carcinogenesis is a traditional, maybe old, way of understanding cancer development. A number of novel approaches are available today to elucidate cancer development. However, there are things we learn from the old, and thus I bring out some examples of various clinical cases and experimental models of foreign-body-induced tumorigenesis. What is notable is that the foreign bodies themselves are unrelated to each other, whereas commonly underlying in them is to induce inflammatory reaction, especially stromal proliferation, where those exogenous materials are incorporated and undigested. Such foreign-body-induced carcinogenesis is also recognized in the step of tumor progression, the final step of carcinogenesis that tumor cells acquire malignant phenotypes including metastatic properties. And the phenomenon is universally observed in several cell lines of different origins. In this review I would like to show the evidence that tumor development and progression are accelerated inevitably by inflammation caused from foreign bodies, and that reactive oxygen species derived from inflammatory cells are one of the most important genotoxic mediators to accelerate the process.

(c) 2007 Wiley-Liss, Inc.

In plain English

This was a review, by a Yamagata University author in Japan, of clinical cases and experimental models linking foreign bodies to tumors. It covered particulate carcinogens such as carbon black and asbestos, metals, medical implants and scar cancers. Its asbestos section drew on other studies and described chrysotile, crocidolite and amosite. It cited an estimated mean mesothelioma latency of 20 to 40 years and mesothelial mutations in rats injected with crocidolite. It also cited an estimated 500 malignant pleural mesothelioma deaths a year in Japan in 1995 to 1999, doubling by 2005. A substantial section summarized the author's group's earlier animal experiments, which used plastic plates and gelatin sponges, not asbestos. In mice, weakly tumorigenic or regressing cells became malignant at foreign-body sites. In a mouse model using QR cells, removing neutrophils prevented malignant features; lacking the gp91phox gene, used to make reactive oxygen species, reduced tumor development and metastatic ability with gelatin sponge. The author concluded that tumor cells' proneness to greater malignancy depends on the balance between their antioxidant enzymes and the reactive oxygen and nitrogen species made by inflammatory cells.

We wrote this plain-English summary from the full article with the help of AI, and a second AI model checked each sentence against the article. It is not the authors' wording; the abstract and the article are their own account.

What the study did and found

• Design: review (narrative review of clinical cases and experimental models, including the author's group's earlier animal and cell experiments)
• Who was studied: No study population of its own; the review discussed human clinical reports and experimental models using cell lines of rat, mouse and human origin implanted in rats and mice
• Exposure: Foreign bodies, including particulate carcinogens (carbon black, asbestos: chrysotile, crocidolite, amosite), metals, medical implants, and, in the author's experiments, polystyrene plastic plates and gelatin sponges
• Main results:
  • The review cited an estimated mean latency of 20 to 40 years from first asbestos exposure to mesothelioma (from other studies)
  • The review cited other researchers' finding of mutations in the mesothelium of rats after injection of crocidolite asbestos
  • The review cited an estimated mean of 500 deaths a year from malignant pleural mesothelioma in Japan between 1995 and 1999, doubling in 2005
  • In the author's group's QR-cell mouse model, mice given an anti-neutrophil antibody (RB6) did not acquire malignant phenotypes
  • In mice lacking the gp91phox gene, the frequency of tumor development from QR cells coimplanted with gelatin sponge was decreased, and acquisition of metastatic ability was reduced
  • Human colonic adenoma cells (FPCK-1-1) attached to plastic plates formed palpable tumors in mice in about 5 months
• The authors' conclusion: The author concluded that the proneness of tumor cells to become more malignant depends on the balance between their own antioxidative enzyme activities and the duration and amount of reactive oxygen and nitrogen species generated by inflammatory cells, and that disturbing this balance would be the most effective prevention strategy

Topics

Medical terms in this study, explained in our Lexicon: Carcinogenesis, Reactive Oxygen Species (ROS), Tumorigenesis, Inflammation.

Related studies

• Mitochondria-derived reactive oxygen species drive GANT61-induced mesothelioma cell apoptosis — C.B. Lim, C.M. Prêle, et al. (2015)
• Reactive oxygen species, chromosome mutation, and cancer: possible role of clastogenic factors in carcinogenesis — I. Emerit (1994)
• The latent form of TGFbeta(1) is induced by TNFalpha through an ERK specific pathway and is activated by asbestos-derived reactive oxygen species in vitro and in vivo — D.E. Sullivan, M. Ferris, et al. (2008)
• Iron and reactive oxygen species in the asbestos-induced tumor necrosis factor-alpha response from alveolar macrophages — P.P. Simeonova, M.I. Luster (1995)
• Carbon nanotubes induce inflammation but decrease the production of reactive oxygen species in lung — D. Crouzier, S. Follot, et al. (2010)
• Mechanisms of the genotoxicity of crocidolite asbestos in mammalian cells: implication from mutation patterns induced by reactive oxygen species — A. Xu, H. Zhou, et al. (2002)

Browse more research in International Journal of Cancer, or return to medical research.