A home-based lifestyle intervention program reduces the tumorigenic potential of triple-negative breast cancer cells.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
29 Jan 2024
29 Jan 2024
Historique:
received:
03
04
2023
accepted:
12
01
2024
medline:
30
1
2024
pubmed:
30
1
2024
entrez:
29
1
2024
Statut:
epublish
Résumé
Translational research for the evaluation of physical activity habits and lifestyle modifications based on nutrition and exercise has recently gained attention. In this study, we evaluated the effects of serum samples obtained before and after a 12-week home-based lifestyle intervention based on nutrition and exercise in breast cancer survivors in terms of modulation of the tumorigenic potential of breast cancer cells. The home-based lifestyle intervention proposed in this work consisted of educational counselling on exercise and nutritional behaviors and in 12 weeks of structured home-based exercise. Triple-negative breast cancer cell line MDA-MB-231 was cultured in semi-solid medium (3D culture) with sera collected before (PRE) and after (POST) the lifestyle intervention program. Spheroid formation was evaluated by counting cell colonies after 3 weeks of incubation. Results show a slight but significant reduction of spheroid formation induced by serum collected POST in comparison to those obtained PRE. Moreover, statistical analyses aimed to find physiologic and metabolic parameters associated with 3D cell proliferation revealed the proliferative inducer IGF-1 as the only predictor of cell tumorigenic potential. These results highlight the importance of lifestyle changes for cancer progression control in a tertiary prevention context. Translational research could offer a useful tool to identify metabolic and physiological changes induced by exercise and nutritional behaviors associated with cancer progression and recurrence risk.
Identifiants
pubmed: 38287041
doi: 10.1038/s41598-024-52065-9
pii: 10.1038/s41598-024-52065-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2409Informations de copyright
© 2024. The Author(s).
Références
Moore, S. C. et al. Association of leisure-time physical activity with risk of 26 types of cancer in 1.44 million adults. JAMA Intern. Med. 176, 816–825 (2016).
pubmed: 27183032
pmcid: 5812009
doi: 10.1001/jamainternmed.2016.1548
Orman, A., Johnson, D. L., Comander, A. & Brockton, N. Breast cancer: A lifestyle medicine approach. Am. J. Lifestyle Med. 14, 483–494 (2020).
pubmed: 32922233
pmcid: 7444002
doi: 10.1177/1559827620913263
Natalucci, V. et al. Effects of a home-based lifestyle intervention program on cardiometabolic health in breast cancer survivors during the covid-19 lockdown. J. Clin. Med. 10, 2678 (2021).
pubmed: 34204528
pmcid: 8235209
doi: 10.3390/jcm10122678
Peterson, L. L. & Ligibel, J. A. Physical activity and breast cancer: An opportunity to improve outcomes. Curr. Oncol. Rep. 20, 1 (2018).
doi: 10.1007/s11912-018-0702-1
Levin, G. T., Greenwood, K. M., Singh, F. & Newton, R. U. Modality of exercise influences rate of decrease in depression for cancer survivors with elevated depressive symptomatology. Support. Care Cancer 26, 1597–1606 (2018).
pubmed: 29204709
Olsson Möller, U., Beck, I., Rydén, L. & Malmström, M. A comprehensive approach to rehabilitation interventions following breast cancer treatment—A systematic review of systematic reviews. BMC Cancer 19, 7 (2019).
doi: 10.1186/s12885-019-5648-7
World Cancer Research Fund/American Institute for Cancer Research. Diet, Nutrition, Physical Activity and Cancer: A Global Perspective. 3rd Export Report. 2018. https://www.wcrf.org/wp-content/uploads/2021/02/Summary-of-%0AThird-Expert-Report-2018.pdf (2018).
Metcalfe, R. S. et al. Anti-carcinogenic effects of exercise-conditioned human serum: Evidence, relevance and opportunities. Eur. J. Appl. Physiol. 121, 2107–2124 (2021).
pubmed: 33864493
pmcid: 8260517
doi: 10.1007/s00421-021-04680-x
Brown, M. J., Morris, M. A. & Akam, E. C. An exploration of the role of exercise in modulating breast cancer progression in vitro: A systematic review and meta-analysis. Am. J. Physiol. Cell Physiol. 320, C253–C263 (2021).
pubmed: 33356943
doi: 10.1152/ajpcell.00461.2020
Orange, S. T., Jordan, A. R. & Saxton, J. M. The serological responses to acute exercise in humans reduce cancer cell growth in vitro: A systematic review and meta-analysis. Physiol. Rep. 8, 635 (2020).
doi: 10.14814/phy2.14635
Yeh, A. C. & Ramaswamy, S. Mechanisms of cancer cell dormancy-another hallmark of cancer? Cancer Res. 75, 5014–5022 (2015).
pubmed: 26354021
pmcid: 4668214
doi: 10.1158/0008-5472.CAN-15-1370
Baldelli, G. et al. The effects of human sera conditioned by high-intensity exercise sessions and training on the tumorigenic potential of cancer cells. Clin. Transl. Oncol. 23, 22–34 (2021).
pubmed: 32447643
doi: 10.1007/s12094-020-02388-6
De Santi, M. et al. A dataset on the effect of exercise-conditioned human sera in three-dimensional breast cancer cell culture. Data Br. 27, 104704 (2019).
doi: 10.1016/j.dib.2019.104704
De Santi, M. et al. Metformin prevents cell tumorigenesis through autophagy-related cell death. Sci. Rep. 9, 6 (2019).
doi: 10.1038/s41598-018-37247-6
Natalucci, V. et al. Movement and health beyond care, MoviS: Study protocol for a randomized clinical trial on nutrition and exercise educational programs for breast cancer survivors. Trials 24, 134 (2023).
pubmed: 36814313
pmcid: 9946288
doi: 10.1186/s13063-023-07153-y
Natalucci, V. et al. Effect of a lifestyle intervention program’s on breast cancer survivors’ cardiometabolic health: Two-year follow-up. Heliyon 9, e21761 (2023).
pubmed: 38027927
pmcid: 10651516
doi: 10.1016/j.heliyon.2023.e21761
Craig, C. L. et al. International physical activity questionnaire: 12-Country reliability and validity. Med. Sci. Sports Exerc. 35, 1381–1395 (2003).
pubmed: 12900694
doi: 10.1249/01.MSS.0000078924.61453.FB
Lee, P. H., Macfarlane, D. J., Lam, T. H. & Stewart, S. M. Validity of the international physical activity questionnaire short form (IPAQ-SF): A systematic review. Int. J. Behav. Nutr. Phys. Act. 8, 115 (2011).
pubmed: 22018588
pmcid: 3214824
doi: 10.1186/1479-5868-8-115
Villarini, A. et al. Lifestyle and breast cancer recurrences: The DIANA-5 trial. Tumori 98, 1–18 (2012).
pubmed: 22495696
doi: 10.1177/030089161209800101
Pistelli, M. et al. Abstract PD11-03: Assessing the impact of 12 months lifestyle interventions on breast cancer secondary prevention: A modeling approach. Cancer Res. 81, 11 (2021).
doi: 10.1158/1538-7445.SABCS20-PD11-03
Rock, C. L. et al. American Cancer Society nutrition and physical activity guideline for cancer survivors. CA Cancer J. Clin. 72, 230–262 (2022).
pubmed: 35294043
doi: 10.3322/caac.21719
Willett, W. C. et al. Mediterranean diet pyramid: A cultural model for healthy eating. Am. J. Clin. Nutr. 61, 1402 (1995).
doi: 10.1093/ajcn/61.6.1402S
Villarini, A., Villarini, M., Gargano, G., Moretti, M. & Berrino, F. DianaWeb: A demonstration project to improve breast cancer prognosis through lifestyles. Epidemiol. Prev. 39, 402–405 (2015).
pubmed: 26554696
Gianfredi, V. et al. E-Coaching: The DianaWeb study to prevent breast cancer recurrences. Clin. Ter. 170, E59–E65 (2020).
pubmed: 31850486
Ferri Marini, C. et al. Assessing maximal oxygen uptake: Creating personalized incremental exercise protocols simply and quickly. Strength Cond. J. 43, 86–92 (2021).
doi: 10.1519/SSC.0000000000000569
American College of Sports Medicine, Riebe, D., Ehrman, J., Liguori, G. & Magal, M. ACSM’s Guidelines for Exercise Testing and Prescription 10th edn. (Wolters Kluwer, 2018).
Gellish, R. L. et al. Longitudinal modeling of the relationship between age and maximal heart rate. Med. Sci. Sports Exerc. 39, 822–829 (2007).
pubmed: 17468581
doi: 10.1097/mss.0b013e31803349c6
Jones, L. W., Eves, N. D., Haykowsky, M., Joy, A. A. & Douglas, P. S. Cardiorespiratory exercise testing in clinical oncology research: Systematic review and practice recommendations. Lancet Oncol. 9, 757–765 (2008).
pubmed: 18672211
doi: 10.1016/S1470-2045(08)70195-5
Friedrich, N. et al. Age- and sex-specific reference intervals across life span for insulin-like growth factor binding protein 3 (IGFBP-3) and the IGF-I to IGFBP-3 ratio measured by new automated chemiluminescence assays. J. Clin. Endocrinol. Metab. 99, 1675–1686 (2014).
pubmed: 24483154
doi: 10.1210/jc.2013-3060
Martínez-González, M. A. et al. A 14-item Mediterranean diet assessment tool and obesity indexes among high-risk subjects: The PREDIMED trial. PLoS ONE 7, e43134 (2012).
pubmed: 22905215
pmcid: 3419206
doi: 10.1371/journal.pone.0043134
Cohen, J., Cohen, P., West, S. G. & Aiken, L. S. Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences 3rd edn, 1–704 (Routledge, 2013).
doi: 10.4324/9780203774441
Clinton, S. K., Giovannucci, E. L. & Hursting, S. D. The World Cancer Research Fund/American Institute for Cancer Research Third Expert Report on diet, nutrition, physical activity, and cancer: Impact and future directions. J. Nutr. 150, 663–671 (2020).
pubmed: 31758189
doi: 10.1093/jn/nxz268
Runowicz, C. D. et al. American Cancer Society/American Society of Clinical Oncology Breast Cancer survivorship care guideline. CA Cancer J. Clin. 66, 43–73 (2016).
pubmed: 26641959
doi: 10.3322/caac.21319
Singh, M., Mukundan, S., Jaramillo, M., Oesterreich, S. & Sant, S. Three-dimensional breast cancer models mimic hallmarks of size-induced tumor progression. Cancer Res. 76, 3702–3710 (2016).
Urzì, O. et al. Three-dimensional cell cultures: The bridge between in vitro and in vivo models. Int. J. Mol. Sci. 24, 12046 (2023).
pubmed: 37569426
pmcid: 10419178
doi: 10.3390/ijms241512046
Dethlefsen, C. et al. Exercise regulates breast cancer cell viability: Systemic training adaptations versus acute exercise responses. Breast Cancer Res. Treat. 159, 469–479 (2016).
pubmed: 27601139
doi: 10.1007/s10549-016-3970-1
Dethlefsen, C. et al. Exercise-induced catecholamines activate the hippo tumor suppressor pathway to reduce risks of breast cancer development. Cancer Res. 77, 4894–4904 (2017).
pubmed: 28887324
doi: 10.1158/0008-5472.CAN-16-3125
Barnard, R. J., Ngo, T. H., Leung, P. S., Aronson, W. J. & Golding, L. A. A low-fat diet and/or strenuous exercise alters the IGF axis in vivo and reduces prostate tumor cell growth in vitro. Prostate 56, 201–206 (2003).
pubmed: 12772189
doi: 10.1002/pros.10251
Barnard, R. J., Gonzalez, J. H., Liva, M. E. & Ngo, T. H. Effects of a low-fat, high-fiber diet and exercise program on breast cancer risk factors in vivo and tumor cell growth and apoptosis in vitro. Nutr. Cancer 55, 28–34 (2006).
pubmed: 16965238
doi: 10.1207/s15327914nc5501_4
Barnard, R. J., Leung, P. S., Aronson, W. J., Cohen, P. & Golding, L. A. A mechanism to explain how regular exercise might reduce the risk for clinical prostate cancer. Eur. J. Cancer Prev. 16, 415–421 (2007).
pubmed: 17923812
doi: 10.1097/01.cej.0000243851.66985.e4
Tymchuk, C. N., Barnard, R. J., Heber, D. & Aronson, W. J. Evidence of an inhibitory effect of diet and exercise on prostate cancer cell growth. J. Urol. 166, 1185–1189 (2001).
pubmed: 11490320
doi: 10.1016/S0022-5347(05)65943-5
Tymchuk, C. N., Barnard, R. J., Ngo, T. H. & Aronson, W. J. Role of testosterone, estradiol, and insulin in diet- and exercise-induced reductions in serum-stimulated prostate cancer cell growth in vitro. Nutr. Cancer 42, 112–116 (2002).
pubmed: 12235642
doi: 10.1207/S15327914NC421_15
Ngo, T. H., Barnard, R. J., Leung, P. S., Cohen, P. & Aronson, W. J. Insulin-like growth factor I (IGF-I) and IGF binding protein-1 modulate prostate cancer cell growth and apoptosis: Possible mediators for the effects of diet and exercise on cancer cell survival. Endocrinology 144, 2319–2324 (2003).
pubmed: 12746292
doi: 10.1210/en.2003-221028
Schwappacher, R. et al. Physical activity and advanced cancer: Evidence of exercise-sensitive genes regulating prostate cancer cell proliferation and apoptosis. J. Physiol. 598, 3871–3889 (2020).
pubmed: 32648302
doi: 10.1113/JP279150
Devin, J. L. et al. Acute high intensity interval exercise reduces colon cancer cell growth. J. Physiol. 597, 2177–2184 (2019).
pubmed: 30812059
pmcid: 6462486
doi: 10.1113/JP277648
Dethlefsen, C., Pedersen, K. S. & Hojman, P. Every exercise bout matters: Linking systemic exercise responses to breast cancer control. Breast Cancer Res. Treat. 162, 399–408 (2017).
pubmed: 28138894
doi: 10.1007/s10549-017-4129-4
Mantzorou, M. et al. Adherence to mediterranean diet and nutritional status in women with breast cancer: What is their impact on disease progression and recurrence-free patients’ survival? Curr. Oncol. 29, 7482–7497 (2022).
pubmed: 36290866
pmcid: 9600150
doi: 10.3390/curroncol29100589
Pannu, M. K. & Constantinou, C. Inflammation, nutrition, and clinical outcomes in breast cancer survivors: A narrative review. Curr. Nutr. Rep. https://doi.org/10.1007/S13668-023-00495-8 (2023).
doi: 10.1007/S13668-023-00495-8
pubmed: 37751147
De Santi, M. et al. Human IGF1 pro-forms induce breast cancer cell proliferation via the IGF1 receptor. Cell. Oncol. 39, 149–159 (2016).
doi: 10.1007/s13402-015-0263-3
Annibalini, G. et al. MIR retroposon exonization promotes evolutionary variability and generates species-specific expression of IGF-1 splice variants. Biochim. Biophys. Acta Gene Regul. Mech. 1859, 757–768 (2016).
doi: 10.1016/j.bbagrm.2016.03.014
Annibalini, G. et al. The intrinsically disordered E-domains regulate the IGF-1 prohormones stability, subcellular localisation and secretion. Sci. Rep. 8, 1–13 (2018).
doi: 10.1038/s41598-018-27233-3
Endogenous Hormones and Breast Cancer Collaborative Group, Key, T. J., Appleby, P. N., Reeves, G. K. & Roddam, A. W. Insulin-like growth factor 1 (IGF1), IGF binding protein 3 (IGFBP3), and breast cancer risk: Pooled individual data analysis of 17 prospective studies. Lancet Oncol. 11, 530–42 (2010).
doi: 10.1016/S1470-2045(10)70095-4
Murphy, N. et al. Insulin-like growth factor-1, insulin-like growth factor-binding protein-3, and breast cancer risk: Observational and Mendelian randomization analyses with ∼ 430,000 women. Ann. Oncol. 31, 641–649 (2020).
pubmed: 32169310
doi: 10.1016/j.annonc.2020.01.066
Rigiracciolo, D. C. et al. IGF-1/IGF-1R/FAK/YAP transduction signaling prompts growth effects in triple-negative breast cancer (TNBC) cells. Cells 9, 1010 (2020).
pubmed: 32325700
pmcid: 7225986
doi: 10.3390/cells9041010
Xue, L. et al. Metformin and an insulin/IGF-1 receptor inhibitor are synergistic in blocking growth of triple-negative breast cancer. Breast Cancer Res. Treat. 185, 73–84 (2021).
pubmed: 32940848
doi: 10.1007/s10549-020-05927-5
Han, J. K. & Kim, G. Role of physical exercise in modulating the insulin-like growth factor system for improving breast cancer outcomes: A meta-analysis. Exp. Gerontol. 152, 111435 (2021).
pubmed: 34098007
doi: 10.1016/j.exger.2021.111435
De Santi, M. et al. Association between metabolic syndrome, insulin resistance, and IGF-1 in breast cancer survivors of DIANA-5 study. J. Cancer Res. Clin. Oncol. 149, 8639–8648 (2023).
pubmed: 37106164
pmcid: 10374719
doi: 10.1007/s00432-023-04755-6
Runchey, S. S. et al. Glycemic load effect on fasting and post-prandial serum glucose, insulin, IGF-1 and IGFBP-3 in a randomized, controlled feeding study. Eur. J. Clin. Nutr. 66, 1146–1152 (2012).
pubmed: 22892437
pmcid: 3463643
doi: 10.1038/ejcn.2012.107
Brand-Miller, J. C., Liu, V., Petocz, P. & Baxter, R. C. The glycemic index of foods influences postprandial insulin-like growth factor-binding protein responses in lean young subjects. Am. J. Clin. Nutr. 82, 350–354 (2005).
pubmed: 16087978
doi: 10.1093/ajcn/82.2.350
de Boer, M. C., Wörner, E. A., Verlaan, D. & van Leeuwen, P. A. M. The mechanisms and effects of physical activity on breast cancer. Clin. Breast Cancer 17, 272–278 (2017).
pubmed: 28233686
doi: 10.1016/j.clbc.2017.01.006
McCormick, B. et al. RTOG 9804: A prospective randomized trial for good-risk ductal carcinoma in situ comparing radiotherapy with observation. J. Clin. Oncol. 33, 709–715 (2015).
pubmed: 25605856
pmcid: 4334775
doi: 10.1200/JCO.2014.57.9029
van Bekkum, S., Drukker, C., van Rosmalen, J., Menke-Pluijmers, M. B. E. & Westenend, P. J. A low risk of recurrence after breast-conserving surgery for DCIS: A single-institution experience. Cancer Treat. Res. Commun. 35, 100706 (2023).
pubmed: 37058969
doi: 10.1016/j.ctarc.2023.100706
Narod, S. A., Iqbal, J., Giannakeas, V., Sopik, V. & Sun, P. Breast cancer mortality after a diagnosis of ductal carcinoma in situ. JAMA Oncol. 1, 888–896 (2015).
pubmed: 26291673
doi: 10.1001/jamaoncol.2015.2510
O’Keefe, T. J., Chau, H., Harismendy, O. & Wallace, A. M. Risk factors for breast cancer mortality after ductal carcinoma in situ diagnosis differ from those for invasive recurrence. Surgery 173, 305–311 (2023).
pubmed: 36435650
doi: 10.1016/j.surg.2022.10.009