Exercise and the Hallmarks of Cancer

Trends in Cancer

Volumn 3, Issue 6, 2017, Pages 423-441

  Ruiz Casado, Ana ^a   Martín Ruiz, Asunción ^a   Pérez, Laura M ^b,c   Provencio, Mariano ^a   Fiuza Luces, Carmen ^c,d   Lucia, Alejandro ^b,c  

^a HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^b UNIVERSIDAD EUROPEA DE MADRID   (Spain)

^c Universidad Complutense   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

immune system; myokines; physical activity; tumor

Indexed keywords

MYOKINE; PROTEIN; UNCLASSIFIED DRUG;

CELL DEATH; ENERGY METABOLISM; EXERCISE; HUMAN; INFLAMMATION; MALIGNANT NEOPLASM; METASTASIS; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR PROMOTION; TUMOR SUPPRESSOR GENE; TUMOR VASCULARIZATION; ANIMAL; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; RISK; SKELETAL MUSCLE;

ANIMALS; CELL DEATH; CELL PROLIFERATION; ENERGY METABOLISM; EXERCISE; GENE EXPRESSION REGULATION; HUMANS; MUSCLE, SKELETAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RISK; SIGNAL TRANSDUCTION;

EID: 85020133311     PISSN: 24058033     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.trecan.2017.04.007     Document Type: Review

References (86)

1. Caspersen, C.J., et al. Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 100 (1985), 126–131.
2. Hallal, P.C., et al. Global physical activity levels: surveillance progress, pitfalls, and prospects. Lancet 380 (2012), 247–257.
3. Robsahm, T.E., et al. Body mass index, physical activity, and colorectal cancer by anatomical subsites: a systematic review and meta-analysis of cohort studies. Eur. J. Cancer Prev. 22 (2013), 492–505.
4. Schmid, D., et al. A systematic review and meta-analysis of physical activity and endometrial cancer risk. Eur. J. Epidemiol. 30 (2015), 397–412.
5. Liu, L., et al. Leisure time physical activity and cancer risk: evaluation of the WHO's recommendation based on 126 high-quality epidemiological studies. Br. J. Sports Med. 50 (2016), 372–378.
6. Liu, Y., et al. Does physical activity reduce the risk of prostate cancer? A systematic review and meta-analysis. Eur. Urol. 60 (2011), 1029–1044.
7. Behrens, G., et al. The association between physical activity and gastroesophageal cancer: systematic review and meta-analysis. Eur. J. Epidemiol. 29 (2014), 151–170.
8. Zhong, S., et al. Nonoccupational physical activity and risk of ovarian cancer: a meta-analysis. Tumour Biol. 35 (2014), 11065–11073.
9. Behrens, G., Leitzmann, M.F., The association between physical activity and renal cancer: systematic review and meta-analysis. Br. J. Cancer 108 (2013), 798–811.
10. Brenner, D.R., et al. Leisure-time physical activity and lung cancer risk: a systematic review and meta-analysis. Lung Cancer 95 (2016), 17–27.
11. Farris, M.S., et al. The association between leisure time physical activity and pancreatic cancer risk in adults: a systematic review and meta-analysis. Cancer Epidemiol. Biomarkers Prev. 24 (2015), 1462–1473.
12. 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 (2016), 816–825.
13. Keum, N., et al. Association of physical activity by type and intensity with digestive system cancer risk. JAMA Oncol. 2 (2016), 1146–1153.
14. Campbell, P.T., et al. Associations of recreational physical activity and leisure time spent sitting with colorectal cancer survival. J. Clin. Oncol. 31 (2013), 876–885.
15. Schmid, D., Leitzmann, M.F., Association between physical activity and mortality among breast cancer and colorectal cancer survivors: a systematic review and meta-analysis. Ann. Oncol. 25 (2014), 1293–1311.
16. Garatachea, N., et al. Elite athletes live longer than the general population: a meta-analysis. Mayo Clin. Proc. 89 (2014), 1195–1200.
17. Pedersen, L., et al. Effects of exercise on tumor physiology and metabolism. Cancer J. 21 (2015), 111–116.
18. Ashcraft, K.A., et al. Efficacy and mechanisms of aerobic exercise on cancer initiation, progression, and metastasis: a critical systematic review of in vivo preclinical data. Cancer Res. 76 (2016), 4032–4050.
19. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
20. Hanahan, D., Weinberg, R.A., The hallmarks of cancer. Cell 100 (2000), 57–70.
21. Low, K.C., Telomerase: central regulator of all of the hallmarks of cancer. Trends Biochem. Sci. 38 (2013), 426–434.
22. Xie, L., et al. Effects of dietary calorie restriction or exercise on the PI3K and Ras signaling pathways in the skin of mice. J. Biol. Chem. 282 (2007), 28025–28035.
23. Zhu, Z., et al. Effects of energy restriction and wheel running on mammary carcinogenesis and host systemic factors in a rat model. Cancer Prev. Res. (Phila.) 5 (2012), 414–422.
24. Kalaany, N.Y., Sabatini, D.M., Tumours with PI3K activation are resistant to dietary restriction. Nature 458 (2009), 725–731.
25. Standard, J., et al. Reduced signaling of PI3K–Akt and RAS–MAPK pathways is the key target for weight-loss-induced cancer prevention by dietary calorie restriction and/or physical activity. J. Nutr. Biochem. 25 (2014), 1317–1323.
26. Colbert, L.H., et al. Exercise effects on tumorigenesis in a p53-deficient mouse model of breast cancer. Med. Sci. Sports Exerc. 41 (2009), 1597–1605.
27. Schiaffino, S., et al. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 280 (2013), 4294–4314.
28. Ouyang, P., et al. Weight loss via exercise with controlled dietary intake may affect phospholipid profile for cancer prevention in murine skin tissues. Cancer Prev. Res. (Phila.) 3 (2010), 466–477.
29. Leung, P.S., et al. Exercise alters the IGF axis in vivo and increases p53 protein in prostate tumor cells in vitro. J. Appl. Physiol. (1985) 96 (2004), 450–454.
30. Yu, M., et al. Exercise activates p53 and negatively regulates IGF-1 pathway in epidermis within a skin cancer model. PLoS One, 11, 2016, e0160939.
31. Piguet, A.C., et al. Regular exercise decreases liver tumors development in hepatocyte-specific PTEN-deficient mice independently of steatosis. J. Hepatol. 62 (2015), 1296–1303.
32. Jiang, W., et al. Effects of physical activity and restricted energy intake on chemically induced mammary carcinogenesis. Cancer Prev. Res. (Phila.) 2 (2009), 338–344.
33. Zhu, Z., et al. Effect of nonmotorized wheel running on mammary carcinogenesis: circulating biomarkers, cellular processes, and molecular mechanisms in rats. Cancer Epidemiol. Biomarkers Prev. 17 (2008), 1920–1929.
34. Min/+ mouse intestinal polyps. J. Appl. Physiol. (1985) 104 (2008), 1137–1143.
35. Khori, V., et al. Effects of exercise training together with tamoxifen in reducing mammary tumor burden in mice: possible underlying pathway of miR-21. Eur. J. Pharmacol. 765 (2015), 179–187.
36. Zheng, X., et al. Inhibitory effect of voluntary running wheel exercise on the growth of human pancreatic Panc-1 and prostate PC-3 xenograft tumors in immunodeficient mice. Oncol. Rep. 19 (2008), 1583–1588.
37. Hojman, P., et al. Exercise-induced muscle-derived cytokines inhibit mammary cancer cell growth. Am. J. Physiol. Endocrinol. Metab. 301 (2011), E504–E510.
38. Barnard, R.J., et al. A mechanism to explain how regular exercise might reduce the risk for clinical prostate cancer. Eur. J. Cancer Prev. 16 (2007), 415–421.
39. Higgins, K.A., et al. Exercise-induced lung cancer regression: mechanistic findings from a mouse model. Cancer 120 (2014), 3302–3310.
40. Betof, A.S., et al. Modulation of murine breast tumor vascularity, hypoxia and chemotherapeutic response by exercise. J. Natl. Cancer Inst., 107, 2015, djv04.
41. Zheng, X., et al. Inhibition of progression of androgen-dependent prostate LNCaP tumors to androgen independence in SCID mice by oral caffeine and voluntary exercise. Nutr. Cancer 64 (2012), 1029–1037.
42. Rudolph, K.L., et al. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat. Genet. 28 (2001), 155–159.
43. Ludlow, A.T., et al. Do telomeres adapt to physiological stress? Exploring the effect of exercise on telomere length and telomere-related proteins. BioMed Res. Int., 2013, 2013, 601368.
44. Mundstock, E., et al. Effects of physical activity in telomere length: systematic review and meta-analysis. Ageing Res. Rev. 22 (2015), 72–80.
45. Shannon, A.M., et al. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat. Rev. 29 (2003), 297–307.
46. Carmeliet, P., Jain, R.K., Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 10 (2011), 417–442.
47. Jones, L.W., et al. Effect of aerobic exercise on tumor physiology in an animal model of human breast cancer. J. Appl. Physiol. (1985) 108 (2010), 343–348.
48. Jones, L.W., et al. Exercise modulation of the host–tumor interaction in an orthotopic model of murine prostate cancer. J. Appl. Physiol. (1985) 113 (2012), 263–272.
49. McCullough, D.J., et al. Modulation of blood flow, hypoxia, and vascular function in orthotopic prostate tumors during exercise. J. Natl. Cancer Inst., 106, 2014, dju036.
50. Verma, V.K., et al. Effect of physical exercise on tumor growth regulating factors of tumor microenvironment: implications in exercise-dependent tumor growth retardation. Immunopharmacol. Immunotoxicol. 31 (2009), 274–282.
51. Shalamzari, S.A., et al. The effect of exercise training on the level of tissue IL-6 and vascular endothelial growth factor in breast cancer bearing mice. Iran. J. Basic Med. Sci 17 (2014), 231–258.
52. Tsai, M.S., et al. The effects of exercise training on levels of vascular endothelial growth factor in tumor-bearing mice. Cancer Biomark. 13 (2013), 307–313.
53. Min/+ mice and azoxymethane/dextran sulfate sodium-treated mice. BMC Cancer, 8, 2008, 316.
54. Zhang, Q.B., et al. Moderate swimming suppressed the growth and metastasis of the transplanted liver cancer in mice model: with reference to nervous system. Oncogene 35 (2016), 4122–4131.
55. Wolff, G., et al. Exercise maintains blood-brain barrier integrity during early stages of brain metastasis formation. Biochem. Biophys. Res. Commun. 463 (2015), 811–817.
56. Jia, W., et al. The role of claudin-5 in blood–brain barrier (BBB) and brain metastases (review). Mol. Med. Rep. 9 (2014), 779–785.
57. Yan, L., Demars, L.C., Effects of non-motorized voluntary running on experimental and spontaneous metastasis in mice. Anticancer Res. 31 (2011), 3337–3344.
58. Almeida, P.W., et al. Swim training suppresses tumor growth in mice. J. Appl. Physiol. (1985) 107 (2009), 261–265.
59. Zielinski, M.R., et al. Exercise delays allogeneic tumor growth and reduces intratumoral inflammation and vascularization. J. Appl. Physiol. (1985) 96 (2004), 2249–2256.
60. Walsh, N.P., et al. Position statement. Part two: maintaining immune health. Exerc. Immunol. Rev. 17 (2011), 64–103.
61. Kruijsen-Jaarsma, M., et al. Effects of exercise on immune function in patients with cancer: a systematic review. Exerc. Immunol. Rev. 19 (2013), 120–143.
62. Zimmer, P., et al. Exercise-induced natural killer cell activation is driven by epigenetic modifications. Int. J. Sports Med. 36 (2015), 510–515.
63. MacNeil, B., Hoffman-Goetz, L., Effect of exercise on natural cytotoxicity and pulmonary tumor metastases in mice. Med. Sci. Sports Exerc. 25 (1993), 922–928.
64. Fairey, A.S., et al. Randomized controlled trial of exercise and blood immune function in postmenopausal breast cancer survivors. J. Appl. Physiol. (1985) 98 (2005), 1534–1540.
65. Nieman, D.C., et al. Moderate exercise training and natural killer cell cytotoxic activity in breast cancer patients. Int. J. Sports Med. 16 (1995), 334–337.
66. Saxton, J.M., et al. Effects of an exercise and hypocaloric healthy eating intervention on indices of psychological health status, hypothalamic–pituitary–adrenal axis regulation and immune function after early-stage breast cancer: a randomised controlled trial. Breast Cancer Res., 16, 2014, R39.
67. Pedersen, L., et al. Voluntary running suppresses tumor growth through epinephrine- and IL-6-dependent NK cell mobilization and redistribution. Cell Metab. 23 (2016), 554–562.
68. Glasner, A., et al. Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1. J. Immunol. 188 (2012), 2509–2515.
69. Lu, Q., et al. Chronic exercise increases macrophage-mediated tumor cytolysis in young and old mice. Am. J. Physiol. 276 (1999), R482–R489.
70. Abdalla, D.R., et al. The influence of physical activity on the profile of immune response cells and cytokine synthesis in mice with experimental breast tumors induced by 7,12-dimethylbenzanthracene. Eur. J. Cancer Prev. 22 (2013), 251–258.
71. Abdalla, D.R., et al. Innate immune response adaptation in mice subjected to administration of DMBA and physical activity. Oncol. Lett. 7 (2014), 886–890.
72. Murphy, E.A., et al. Effects of moderate exercise and oat beta-glucan on lung tumor metastases and macrophage antitumor cytotoxicity. J. Appl. Physiol. (1985) 97 (2004), 955–959.
73. Rolny, C., et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19 (2011), 31–44.
74. Ruffell, B., et al. Differential macrophage programming in the tumor microenvironment. Trends Immunol. 33 (2012), 119–126.
75. Goh, J., et al. Exercise training in transgenic mice is associated with attenuation of early breast cancer growth in a dose-dependent manner. PLoS One, 8, 2013, e80123.
76. Min/+ mouse model of intestinal tumorigenesis. Int. J. Oncol. 45 (2014), 861–868.
77. Hampras, S.S., et al. Predictors of immunosuppressive regulatory T lymphocytes in healthy women. J. Cancer Epidemiol., 2012, 2012, 191090.
78. Davis, J.M., et al. Exercise effects on lung tumor metastases and in vitro alveolar macrophage antitumor cytotoxicity. Am. J. Physiol. 274 (1998), R1454–R1459.
79. Fiuza-Luces, C., et al. Exercise is the real polypill. Physiology (Bethesda) 28 (2013), 330–358.
80. Aoi, W., et al. A novel myokine, secreted protein acidic and rich in cysteine (SPARC), suppresses colon tumorigenesis via regular exercise. Gut 62 (2013), 882–889.
81. Dethlefsen, C., et al. Every exercise bout matters: linking systemic exercise responses to breast cancer control. Breast Cancer Res. Treat. 162 (2017), 399–408.
82. Pedersen, B.K., Febbraio, M.A., Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev. 88 (2008), 1379–1406.
83. Stone, R.L., et al. Paraneoplastic thrombocytosis in ovarian cancer. N. Engl. J. Med. 366 (2012), 610–618.
84. Schmitz, K.H., et al. American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. Med. Sci. Sports Exerc. 42 (2010), 1409–1426.
85. Campbell, S.C., Wisniewski, P.J. II, Exercise is a novel promoter of intestinal health and microbial diversity. Exerc. Sport Sci. Rev. 45 (2016), 41–47.
86. Honda, K., Littman, D.R., The microbiota in adaptive immune homeostasis and disease. Nature 535 (2016), 75–84.