Effects of physical activity on systemic oxidative/DNA status in breast cancer survivors

Tomasello,Barbara; Malfa,Giuseppe Antonio; Strazzanti,Angela; Gangi,Santi; Di Giacomo,Claudia; Basile,Francesco; Renis,Marcella

doi:10.3892/ol.2016.5449

Effects of physical activity on systemic oxidative/DNA status in breast cancer survivors

Authors:
- Barbara Tomasello
- Giuseppe Antonio Malfa
- Angela Strazzanti
- Santi Gangi
- Claudia Di Giacomo
- Francesco Basile
- Marcella Renis
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Affiliations: Department of Drug Sciences, Section of Biochemistry, University of Catania, I‑95125 Catania, Italy, Department of Surgery, University of Catania, I‑95124 Catania, Italy
Published online on: November 30, 2016 https://doi.org/10.3892/ol.2016.5449
Pages: 441-448

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Abstract

Physical activity offers a paradoxical hormetic effect and a health benefit to cancer survivors; however, the biochemical mechanisms have not been entirely elucidated. Despite the well‑documented evidence implicating oxidative stress in breast cancer, the association between health benefits and redox status has not been investigated in survivors who participate in dragon boating. The present study investigated the plasmatic systemic oxidative status (SOS) in breast cancer survivors involved in two distinct physical training exercises. A total of 75 breast cancer survivors were allocated to one of three groups: Control (resting), dragon boat racing and walking group; the latter is a type of aerobic conditioning exercise often advised to cancer patients. Various biochemical oxidative stress markers were examined, including oxidant status (hydroperoxide levels, lipid oxidation) and antioxidant status (enzymatic activities of superoxide dismutase and glutathione peroxidase, reduced glutathione levels and antioxidant capability). In addition, the individual DNA fragmentation and DNA repair capability of nucleotide excision repair (NER) systems were examined by comet assays. According to the results, all patients exhibited high levels of oxidative stress. Physical activity maintained this oxidative stress condition but simultaneously had a positive influence on the antioxidant component of the SOS, particularly in the dragon boat racing group. DNA fragmentation, according to the levels of single‑ and double‑strand breaks, were within the normal range in the two survivor groups that were involved in training activities. Radiation‑induced damage was not completely recognised or repaired by NER systems in any of the patients, probably leading to radiosensitivity and/or susceptibility of patients to cancer. These findings suggest that physical activity, particularly dragon boat racing, that modulates SOS and DNA repair capability could represent a strategy for enhancing the quality of life and improving the long‑term health benefits for breast cancer survivors.

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1	Carlson RW, Allred DC, Anderson BO, Burstein HJ, Carter WB, Edge SB, Erban JK, Farrar WB, Goldstein LJ, Gradishar WJ, et al: Breast cancer. Clinical practice guidelines in oncology. J Natl Compr Canc Netw. 7:122–192. 2009.PubMed/NCBI
2	Acharya A, Das I, Chandhok D and Saha T: Redox regulation in cancer: A double-edged sword with therapeutic potential. Oxid Med Cell Longev. 3:23–34. 2010. View Article : Google Scholar : PubMed/NCBI
3	Martin KR and Barrett JC: Reactive oxygen species as double-edged swords in cellular processes: Low-dose cell signaling versus high-dose toxicity. Hum Exp Toxicol. 21:71–75. 2002. View Article : Google Scholar : PubMed/NCBI
4	Cooke MS, Evans MD, Dizdaroglu M and Lunec J: Oxidative DNA damage: Mechanisms, mutation, and disease. FASEB J. 17:1195–1214. 2003. View Article : Google Scholar : PubMed/NCBI
5	Klaunig JE, Kamendulis LM and Hocevar BA: Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol. 38:96–109. 2010. View Article : Google Scholar : PubMed/NCBI
6	Scott TL, Rangaswamy S, Wicker CA and Izumi T: Repair of oxidative DNA damage and cancer: Recent progress in DNA base excision repair. Antioxid Redox Signal. 20:708–726. 2014. View Article : Google Scholar : PubMed/NCBI
7	McCausland LL: Dragon boat racing: Life after breast cancer treatment. Am J Nurs. 110:48–54. 2010. View Article : Google Scholar : PubMed/NCBI
8	Hull MM: Lymphedema in women treated for breast cancer. Semin Oncol Nurs. 16:226–237. 2000. View Article : Google Scholar : PubMed/NCBI
9	Bouillet T, Bigard X, Brami C, Chouahnia K, Copel L, Dauchy S, Delcambre C, Descotes JM, Joly F, Lepeu G, et al: Role of physical activity and sport in oncology: Scientific commission of the National Federation Sport and Cancer CAMI. Crit Rev Oncol Hematol. 94:74–86. 2015. View Article : Google Scholar : PubMed/NCBI
10	Knop K, Schwan R, Bongartz M, Bloch W, Brixius K and Baumann F: Sport and oxidative stress in oncological patients. Int J Sports Med. 32:960–964. 2011. View Article : Google Scholar : PubMed/NCBI
11	McCullough LE, Santella RM, Cleveland RJ, Bradshaw PT, Millikan RC, North KE, Olshan AF, Eng SM, Ambrosone CB, Ahn J, et al: Polymorphisms in oxidative stress genes, physical activity, and breast cancer risk. Cancer Causes Control. 23:1949–958. 2012. View Article : Google Scholar : PubMed/NCBI
12	NLN Medical Advisory Committee, . Position statement of the National Lymphedema Network: exercise. San Francisco: National Lymphedema Network; 2013
13	Trotti R, Carratelli M and Barbieri M: Performance and clinical application of a new, fast method for the detection of hydroperoxides in serum. Panminerva Med. 44:37–40. 2002.PubMed/NCBI
14	Benzie IF and Strain JJ: The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: The FRAP assay. Anal Biochem. 239:70–76. 1996. View Article : Google Scholar : PubMed/NCBI
15	Di Giacomo C, Acquaviva R, Sorrenti V, Vanella A, Grasso S, Barcellona ML, Galvano F, Vanella L and Renis M: Oxidative and antioxidant status in plasma of runners: Effect of oral supplementation with natural antioxidants. J Med Food. 12:145–150. 2009. View Article : Google Scholar : PubMed/NCBI
16	Paglia DE and Valentine WN: Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 70:158–169. 1967.PubMed/NCBI
17	Sandström J, Nilsson P, Karlsson K and Marklund SL: 10-fold increase in human plasma extracellular superoxide dismutase content caused by a mutation in heparin-binding domain. J Biol Chem. 269:19163–19166. 1994.PubMed/NCBI
18	Tomasello B, Grasso S, Malfa G, Stella S, Favetta M and Renis M: Double-face activity of resveratrol in voluntary runners: Assessment of DNA damage by comet assay. J Med Food. 15:441–447. 2012. View Article : Google Scholar : PubMed/NCBI
19	European Standards Committee on Oxidative DNA Damage (ESCODD), . Measurement of DNA oxidation in human cells by chromatographic and enzymic methods. Free Radic Biol Med. 34:1089–1099. 2003. View Article : Google Scholar : PubMed/NCBI
20	Russo A, Palumbo M, Aliano C, Lempereur L, Scoto G and Renis M: Red wine micronutrients as protective agents in Alzheimer-like induced insult. Life Sci. 72:2369–2379. 2003. View Article : Google Scholar : PubMed/NCBI
21	Collins AR, Dusinská M, Horváthová E, Munro E, Savio M and Stĕtina R: Inter-individual differences in repair of DNA base oxidation, measured in vitro with the comet assay. Mutagenesis. 16:297–301. 2001. View Article : Google Scholar : PubMed/NCBI
22	Gaivão I, Piasek A, Brevik A, Shaposhnikov S and Collins AR: Comet assay-based methods for measuring DNA repair in vitro; estimates of inter- and intra-individual variation. Cell Biol Toxicol. 25:45–52. 2009. View Article : Google Scholar : PubMed/NCBI
23	Harris SR and Niesen-Vertommen SL: Challenging the myth of exercise-induced lymphedema following breast cancer: A series of case reports. J Surg Oncol. 74:95–99. 2000. View Article : Google Scholar : PubMed/NCBI
24	Fu MR, Ridner SH and Armer J: Post-breast cancer. Lymphedema: Part 1. Am J Nurs. 109:48–54; quiz 55. 2009. View Article : Google Scholar : PubMed/NCBI
25	Mandelblatt JS, Luta G, Kwan ML, Makgoeng SB, Ergas IJ, Roh JM, Sternfeld B, Adams-Campbell LL and Kushi LH: Associations of physical activity with quality of life and functional ability in breast cancer patients during active adjuvant treatment: The Pathways Study. Breast Cancer Res Treat. 129:521–529. 2011. View Article : Google Scholar : PubMed/NCBI
26	Vera-Ramirez L, Sanchez-Rovira P, Ramirez-Tortosa MC, Ramirez-Tortosa CL, Granados-Principal S, Lorente JA and Quiles JL: Free radicals in breast carcinogenesis, breast cancer progression and cancer stem cells. Biological bases to develop oxidative-based therapies. Crit Rev Oncol Hematol. 80:347–368. 2011. View Article : Google Scholar : PubMed/NCBI
27	Aslan R, Kutlu R, Civi S and Tasyurek E: The correlation of the total antioxidant status (TAS), total oxidant status (TOS) and paraoxonase activity (PON1) with smoking. Clin Biochem. 47:393–397. 2014. View Article : Google Scholar : PubMed/NCBI
28	Shen J, Gammon MD, Terry MB, Wang Q, Bradshaw P, Teitelbaum SL, Neugut AI and Santella RM: Telomere length, oxidative damage, antioxidants and breast cancer risk. Int J Cancer. 124:1637–1643. 2009. View Article : Google Scholar : PubMed/NCBI
29	Fortner RT, Tworoger SS, Wu T and Eliassen AH: Plasma florescent oxidation products and breast cancer risk: Repeated measures in the Nurses' Health Study. Breast Cancer Res Treat. 141:307–316. 2013. View Article : Google Scholar : PubMed/NCBI
30	Rajneesh CP, Manimaran A, Sasikala KR and Adaikappan P: Lipid peroxidation and antioxidant status in patients with breast cancer. Singapore Med J. 49:640–643. 2008.PubMed/NCBI
31	Abiaka C, Al-Awadi F, Al-Sayer H, Gulshan S, Behbehani A and Farghally M: Activities of erythrocyte antioxidant enzymes in cancer patients. J Clin Lab Anal. 16:167–171. 2002. View Article : Google Scholar : PubMed/NCBI
32	Kasapović J, Pejić S, Todorović A, Stojiljković V and Pajović SB: Antioxidant status and lipid peroxidation in the blood of breast cancer patients of different ages. Cell Biochem Funct. 26:723–730. 2008. View Article : Google Scholar : PubMed/NCBI
33	Hasan HR, Mathkor TH and Al-Habal MH: Superoxide dismutase isoenzyme activities in plasma and tissues of Iraqi patients with breast cancer. Asian Pac J Cancer Prev. 13:2571–2576. 2012. View Article : Google Scholar : PubMed/NCBI
34	Gago-Dominguez M, Jiang X and Castelao J Esteban: Lipid peroxidation and the protective effect of physical exercise on breast cancer. Med Hypotheses. 68:1138–1143. 2007. View Article : Google Scholar : PubMed/NCBI
35	Balneaves LG, Van Patten C, Truant TL, Kelly MT, Neil SE and Campbell KL: Breast cancer survivors' perspectives on a weight loss and physical activity lifestyle intervention. Support Care Cancer. 22:2057–65. 2014.PubMed/NCBI
36	Carter CL, Onicescu G, Cartmell KB, Sterba KR, Tomsic J, Fox T, Dunmeyer E and Alberg AJ: Factors associated with cancer survivors' selection between two group physical activity programs. J Cancer Surviv. 4:388–398. 2010. View Article : Google Scholar : PubMed/NCBI
37	Kobayashi M and Yamamoto M: Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal. 7:385–394. 2005. View Article : Google Scholar : PubMed/NCBI
38	Carayol M, Romieu G, Bleuse JP, Senesse P, Gourgou-Bourgade S, Sari C, Jacot W, Sancho-Garnier H, Janiszewski C, Launay S, et al: Adapted physical activity and diet (APAD) during adjuvant breast cancer therapy: Design and implementation of a prospective randomized controlled trial. Contemp Clin Trials. 36:531–543. 2013. View Article : Google Scholar : PubMed/NCBI
39	Sánchez P, Peñarroja R, Gallegos F, Bravo JL, Rojas E and Benítez-Bribiesca L: DNA damage in peripheral lymphocytes of untreated breast cancer patients. Arch Med Res. 35:480–483. 2004. View Article : Google Scholar : PubMed/NCBI
40	Hussien MM, McNulty H, Armstrong N, Johnston PG, Spence RA and Barnett Y: Investigation of systemic folate status, impact of alcohol intake and levels of DNA damage in mononuclear cells of breast cancer patients. Br J Cancer. 92:1524–1530. 2005. View Article : Google Scholar : PubMed/NCBI
41	Shahidi M, Mozdarani H and Bryant PE: Radiation sensitivity of leukocytes from healthy individuals and breast cancer patients as measured by the alkaline and neutral comet assay. Cancer Lett. 257:263–273. 2007. View Article : Google Scholar : PubMed/NCBI
42	Mao Z, Hine C, Tian X, Van Meter M, Au M, Vaidya A, Seluanov A and Gorbunova V: SIRT6 promotes DNA repair under stress by activating PARP1. Science. 332:1443–1446. 2011. View Article : Google Scholar : PubMed/NCBI