The effects of muscle factors irisin on lipid metabolism in breast cancer: A possible mechanism anti-tumor mechanism of physical activity

  • Jiaxin Zhu College of Physical Education, Shandong Normal University, Jinan 250000, China
  • Chengxiang Li College of Physical Education, Shandong Normal University, Jinan 250000, China
  • Siyu Tian College of Physical Education, Shandong Normal University, Jinan 250000, China
  • Meng Ding College of Physical Education, Shandong Normal University, Jinan 250000, China
Keywords: irisin; adipocyte; cancer-associated adipocytes; breast cancer; cancer
Ariticle ID: 345

Abstract

Breast cancer is the most prevalent cancer in the female population and is a significant cause of global cancer deaths in this group. Obesity increases a woman’s risk of developing breast cancer and has a negative impact on prognosis. Metabolic alterations are an important part of the process of cancer migration; invasion and proliferation, with lipids being a major metabolic substrate for rapid cancer progression, capable of influencing the metabolic crosstalk between tumor cells and other cells in the tumor microenvironment. Physical activity-induced irisin affects the progression of obesity-associated breast cancer and is a new indicator for breast cancer diagnosis. Existing evidence suggests a potential inhibitory effect of physical activity-induced irisin on the progression of breast cancer. A strong association exists between obesity and breast cancer progression and outcomes. This paper discusses how physical activity-induced irisin may achieve cancer suppression by affecting lipid metabolic processes between breast cancer cells and cancer-associated adipocytes, and elucidates the molecular pathways involved in the effects of irisin on cancer lipid reprogramming, thereby helping to prevent the metastatic progression of breast cancer, and ultimately improving the survival rate of this patient group.

References

1. Bray, F., Laversanne, M., Sung, H., Ferlay, J., Siegel, R. L., Soerjomataram, I., & Jemal, A. (2024). Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 74(3), 229-263. doi:10.3322/caac.21834

2. Yin, L., Duan, J. J., Bian, X. W., & Yu, S. C. (2020). Triple-negative breast cancer molecular subtyping and treatment progress. Breast Cancer Res, 22(1), 61. doi:10.1186/s13058-020-01296-5

3. Kaul, K., Misri, S., Ramaswamy, B., & Ganju, R. K. (2021). Contribution of the tumor and obese microenvironment to triple negative breast cancer. Cancer Lett, 509, 115-120. doi:10.1016/j.canlet.2021.03.024

4. Papakonstantinou, E., Piperigkou, Z., Karamanos, N. K., & Zolota, V. (2022). Altered Adipokine Expression in Tumor Microenvironment Promotes Development of Triple Negative Breast Cancer. Cancers (Basel), 14(17). doi:10.3390/cancers14174139

5. Zhao, C., Wu, M., Zeng, N., Xiong, M., Hu, W., Lv, W., . . . Wu, Y. (2020). Cancer-associated adipocytes: emerging supporters in breast cancer. J Exp Clin Cancer Res, 39(1), 156. doi:10.1186/s13046-020-01666-z

6. Speck, R. M., Courneya, K. S., Mâsse, L. C., Duval, S., & Schmitz, K. H. (2010). An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. J Cancer Surviv, 4(2), 87-100. doi:10.1007/s11764-009-0110-5

7. Provatopoulou, X., Georgiou, G. P., Kalogera, E., Kalles, V., Matiatou, M. A., Papapanagiotou, I., . . . Gounaris, A. (2015). Serum irisin levels are lower in patients with breast cancer: association with disease diagnosis and tumor characteristics. BMC Cancer, 15, 898. doi:10.1186/s12885-015-1898-1

8. Zhang, Z. P., Zhang, X. F., Li, H., Liu, T. J., Zhao, Q. P., Huang, L. H., . . . Hao, D. J. (2018). Serum irisin associates with breast cancer to spinal metastasis. Medicine (Baltimore), 97(17), e0524. doi:10.1097/md.0000000000010524

9. Roca-Rivada, A., Castelao, C., Senin, L. L., Landrove, M. O., Baltar, J., Belén Crujeiras, A., . . . Pardo, M. (2013). FNDC5/irisin is not only a myokine but also an adipokine. PLoS One, 8(4), e60563. doi:10.1371/journal.pone.0060563

10. Huh, J. Y., Panagiotou, G., Mougios, V., Brinkoetter, M., Vamvini, M. T., Schneider, B. E., & Mantzoros, C. S. (2012). FNDC5 and irisin in humans: I. Predictors of circulating concentrations in serum and plasma and II. mRNA expression and circulating concentrations in response to weight loss and exercise. Metabolism, 61(12), 1725-1738. doi: 10.1016/j.metabol.2012.09.002

11. Aydin, S., Kuloglu, T., Aydin, S., Kalayci, M., Yilmaz, M., Cakmak, T., . . . Ozercan, I. H. (2014). A comprehensive immunohistochemical examination of the distribution of the fat-burning protein irisin in biological tissues. Peptides, 61, 130-136. doi: 10.1016/j.peptides.2014.09.014

12. Liu S, Du F, Li X, et al. Effects and underlying mechanisms of Irisin on the proliferation and apoptosis of pancreatic 50β cells[J]. PloS one, 2017, 12(4): e0175498.

13. Mazur-Bialy, A. I., Pocheć, E., & Zarawski, M. (2017). Anti-Inflammatory Properties of Irisin, Mediator of Physical Activity, Are Connected with TLR4/MyD88 Signaling Pathway Activation. Int J Mol Sci, 18(4). doi:10.3390/ijms18040701

14. Li, H., Zhang, Y., Wang, F., Donelan, W., Zona, M. C., Li, S., . . . Yang, L. (2019). Effects of irisin on the differentiation and browning of human visceral white adipocytes. Am J Transl Res, 11(12), 7410-7421.

15. Dong, J., Dong, Y., Dong, Y., Chen, F., Mitch, W. E., & Zhang, L. (2016). Inhibition of myostatin in mice improves insulin sensitivity via irisin-mediated cross talk between muscle and adipose tissues. Int J Obes (Lond), 40(3), 434-442. doi:10.1038/ijo.2015.200

16. Lee, Y., Park, S., Park, S., Kwon, H. J., Lee, S. H., Kim, Y., & Kim, J. H. (2024). Exercise affects high-fat diet-stimulated breast cancer metastasis through irisin secretion by altering cancer stem cell properties. Biochem Biophys Rep, 38, 101684. doi: 10.1016/j.bbrep.2024.101684

17. Gannon, N. P., Vaughan, R. A., Garcia-Smith, R., Bisoffi, M., & Trujillo, K. A. (2015). Effects of the physical activity-inducible myokine irisin on malignant and nonmalignant breast epithelial cell behavior in vitro. Int J Cancer, 136(4), E197-202. doi:10.1002/ijc.29142

18. Coletta, A. M., Agha, N. H., Baker, F. L., Niemiro, G. M., Mylabathula, P. L., Brewster, A. M., . . . Simpson, R. J. (2021). The impact of high-intensity interval physical activity training on NK-cell function and circulating myokines for breast cancer prevention among women at high risk for breast cancer. Breast Cancer Res Treat, 187(2), 407-416. doi:10.1007/s10549-021-06111-z

19. Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 68(6), 394-424. doi:10.3322/caac.21492

20. Rafiemanesh, H., Salehiniya, H., & Lotfi, Z. (2016). Breast Cancer in Iranian Woman: Incidence by Age Group, Morphology and Trends. Asian Pac J Cancer Prev, 17(3), 1393-1397. doi:10.7314/apjcp.2016.17.3.1393

21. Tan, M. M., Ho, W. K., Yoon, S. Y., Mariapun, S., Hasan, S. N., Lee, D. S., . . . Teo, S. H. (2018). A case‒control study of breast cancer risk factors in 7,663 women in Malaysia. PLoS One, 13(9), e0203469. doi:10.1371/journal.pone.0203469

22. Brody, J. G., Moysich, K. B., Humblet, O., Attfield, K. R., Beehler, G. P., & Rudel, R. A. (2007). Environmental pollutants and breast cancer: epidemiologic studies. Cancer, 109(12 Suppl), 2667-2711. doi:10.1002/cncr.22655

23. Walsh, T., Lee, M. K., Casadei, S., Thornton, A. M., Stray, S. M., Pennil, C., . . . King, M. C. (2010). Detection of inherited mutations for breast and ovarian cancer using genomic capture and massively parallel sequencing. Proc Natl Acad Sci U S A, 107(28), 12629-12633. doi:10.1073/pnas.1007983107

24. Macacu, A., Autier, P., Boniol, M., & Boyle, P. (2015). Active and passive smoking and risk of breast cancer: a meta-analysis. Breast Cancer Res Treat, 154(2), 213-224. doi:10.1007/s10549-015-3628-4

25. Hiller, T. W. R., O'Sullivan, D. E., Brenner, D. R., Peters, C. E., & King, W. D. (2020). Solar Ultraviolet Radiation and Breast Cancer Risk: A Systematic Review and Meta-Analysis. Environ Health Perspect, 128(1), 16002. doi:10.1289/ehp4861

26. Zhou, X., Yu, L., Wang, L., Xiao, J., Sun, J., Zhou, Y., . . . Li, X. (2022). Alcohol consumption, blood DNA methylation and breast cancer: a Mendelian randomization study. Eur J Epidemiol, 37(7), 701-712. doi:10.1007/s10654-022-00886-1

27. Maccora, J., Garland, S. N., Ftanou, M., Day, D., White, M., Lopez, V. A., . . . Wiley, J. F. (2022). The Sleep, Cancer and Rest (SleepCaRe) Trial: Rationale and design of a randomized, controlled trial of cognitive behavioral and bright light therapy for insomnia and fatigue in women with breast cancer receiving chemotherapy. Contemp Clin Trials, 120, 106877. doi: 10.1016/j.cct.2022.106877

28. de Boer, M. C., Wörner, E. A., Verlaan, D., & van Leeuwen, P. A. M. (2017). The Mechanisms and Effects of Physical Activity on Breast Cancer. Clin Breast Cancer, 17(4), 272-278. doi:10.1016/j.clbc.2017.01.006

29. Nounu, A., Kar, S. P., Relton, C. L., & Richmond, R. C. (2022). Sex steroid hormones and risk of breast cancer: a two-sample Mendelian randomization study. Breast Cancer Res, 24(1), 66. doi:10.1186/s13058-022-01553-9

30. Chan, D. S. M., Vieira, A. R., Aune, D., Bandera, E. V., Greenwood, D. C., McTiernan, A., . . . Norat, T. (2014). Body mass index and survival in women with breast cancer-systematic literature review and meta-analysis of 82 follow-up studies. Ann Oncol, 25(10), 1901-1914. doi:10.1093/annonc/mdu042

31. Lee, K., Kruper, L., Dieli-Conwright, C. M., & Mortimer, J. E. (2019). The Impact of Obesity on Breast Cancer Diagnosis and Treatment. Curr Oncol Rep, 21(5), 41. doi:10.1007/s11912-019-0787-1

32. Matthews, S. B., & Thompson, H. J. (2016). The Obesity-Breast Cancer Conundrum: An Analysis of the Issues. Int J Mol Sci, 17(6). doi:10.3390/ijms17060989

33. Go, Y., Chung, M., & Park, Y. (2016). Dietary Patterns for Women With Triple-negative Breast Cancer and Dense Breasts. Nutr Cancer, 68(8), 1281-1288. doi:10.1080/01635581.2016.1225102

34. Pang, Y., Wei, Y., & Kartsonaki, C. (2022). Associations of adiposity and weight change with recurrence and survival in breast cancer patients: a systematic review and meta-analysis. Breast Cancer, 29(4), 575-588. doi:10.1007/s12282-022-01355-z

35. Dowsett, M., & Folkerd, E. (2015). Reduced progesterone levels explain the reduced risk of breast cancer in obese premenopausal women: a new hypothesis. Breast Cancer Res Treat, 149(1), 1-4. doi:10.1007/s10549-014-3211-4

36. Laudisio, D., Muscogiuri, G., Barrea, L., Savastano, S., & Colao, A. (2018). Obesity and breast cancer in premenopausal women: Current evidence and future perspectives. Eur J Obstet Gynecol Reprod Biol, 230, 217-221. doi: 10.1016/j.ejogrb.2018.03.050

37. Tan, X. J., Cheor, W. L., Cheng, E. M., Rahman, K. S. A., Muhamad, W. Z. A. W., & Leow, W. Z. (2023). Breast cancer status, grading system, etiology, and challenges in Asia: an updated review. Oncologie, 25(2), 99-110. Retrieved from https://doi.org/10.1515/oncologie-2022-1011. doi:doi:10.1515/oncologie-2022-1011

38. Pierobon, M., & Frankenfeld, C. L. (2013). Obesity as a risk factor for triple-negative breast cancers: a systematic review and meta-analysis. Breast Cancer Res Treat, 137(1), 307-314. doi:10.1007/s10549-012-2339-3

39. Yang, X. R., Chang-Claude, J., Goode, E. L., Couch, F. J., Nevanlinna, H., Milne, R. L., . . . Garcia-Closas, M. (2011). Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst, 103(3), 250-263. doi:10.1093/jnci/djq526

40. Cha, Y. J., & Koo, J. S. (2018). Adipokines as therapeutic targets in breast cancer treatment. Expert Opin Ther Targets, 22(11), 941-953. doi:10.1080/14728222.2018.1538356

41. Laplane, L., Duluc, D., Larmonier, N., Pradeu, T., & Bikfalvi, A. (2018). The Multiple Layers of the Tumor Environment. Trends Cancer, 4(12), 802-809. doi: 10.1016/j.trecan. 2018.10.002

42. Moon, H. G., Han, W., & Noh, D. Y. (2009). Underweight and breast cancer recurrence and death: a report from the Korean Breast Cancer Society. J Clin Oncol, 27(35), 5899-5905. doi:10.1200/jco.2009.22.4436

43. Dirat, B., Bochet, L., Dabek, M., Daviaud, D., Dauvillier, S., Majed, B., . . . Muller, C. (2011). Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res, 71(7), 2455-2465. doi:10.1158/0008-5472.Can-10-3323

44. Wang, Y. Y., Lehuédé, C., Laurent, V., Dirat, B., Dauvillier, S., Bochet, L., . . . Muller, C. (2012). Adipose tissue and breast epithelial cells: a dangerous dynamic duo in breast cancer. Cancer Lett, 324(2), 142-151. doi:10.1016/j.canlet.2012.05.019

45. Dumas, J. F., & Brisson, L. (2021). Interaction between adipose tissue and cancer cells: role for cancer progression. Cancer Metastasis Rev, 40(1), 31-46. doi:10.1007/s10555-020-09934-2

46. Zhao, C., Wu, M., Zeng, N., Xiong, M., Hu, W., Lv, W., . . . Wu, Y. (2020). Cancer-associated adipocytes: emerging supporters in breast cancer. J Exp Clin Cancer Res, 39(1), 156. doi:10.1186/s13046-020-01666-z

47. Wang, Z., Jiang, Q., & Dong, C. (2020). Metabolic reprogramming in triple-negative breast cancer. Cancer Biol Med, 17(1), 44-59. doi:10.20892/j.issn.2095-3941.2019.0210

48. Grabner, G. F., Xie, H., Schweiger, M., & Zechner, R. (2021). Lipolysis: cellular mechanisms for lipid mobilization from fat stores. Nat Metab, 3(11), 1445-1465. doi:10.1038/s42255-021-00493-6

49. Cao, Y. (2019). Adipocyte and lipid metabolism in cancer drug resistance. J Clin Invest, 129(8), 3006-3017. doi:10.1172/jci127201

50. Attané, C., & Muller, C. (2020). Drilling for Oil: Tumor-Surrounding Adipocytes Fueling Cancer. Trends Cancer, 6(7), 593-604. doi:10.1016/j.trecan.2020.03.001

51. Balaban, S., Shearer, R. F., Lee, L. S., van Geldermalsen, M., Schreuder, M., Shtein, H. C., . . . Hoy, A. J. (2017). Adipocyte lipolysis links obesity to breast cancer growth: adipocyte-derived fatty acids drive breast cancer cell proliferation and migration. Cancer Metab, 5, 1. doi:10.1186/s40170-016-0163-7

52. Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., . . . Spiegelman, B. M. (2012). A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature, 481(7382), 463-468. doi:10.1038/nature10777

53. Gannon, N. P., Vaughan, R. A., Garcia-Smith, R., Bisoffi, M., & Trujillo, K. A. (2015). Effects of the exercise-inducible myokine irisin on malignant and non-malignant breast epithelial cell behavior in vitro. Int J Cancer, 136(4), E197-202. doi:10.1002/ijc.29142

54. Kuloglu, T., Celik, O., Aydin, S., Hanifi Ozercan, I., Acet, M., Aydin, Y., . . . Kocaman, N. (2016). Irisin immunostaining characteristics of breast and ovarian cancer cells. Cell Mol Biol (Noisy-le-grand), 62(8), 40-44.

55. Panagiotou, G., Triantafyllidou, S., Tarlatzis, B. C., & Papakonstantinou, E. (2021). Serum Levels of Irisin and Omentin-1 in Breast Neoplasms and Their Association with Tumor Histology. Int J Endocrinol, 2021, 6656671. doi:10.1155/2021/6656671

56. Cebulski, K., Piotrowska, A., Kmiecik, A., Haczkiewicz-Leśniak, K., Ciesielska, U., Grzegrzółka, J., . . . Nowińska, K. (2023). The Role of Irisin/FNDC5 Expression and Its Serum Level in Breast Cancer. Int J Mol Sci, 24(10). doi:10.3390/ijms24108628

57. Tejeda, M. E., Canto, P., Tenorio-Torres, A., Orozco-Arguelles, L., Coral-Vázquez, R. M., Zentella-Dehesa, A., . . . Méndez, J. P. (2021). Increased FNDC5/IRISIN protein expression in breast cancer tissue is associated with obesity in postmenopausal women. J Clin Pathol. doi:10.1136/jclinpath-2020-207249

58. Cannon, B., & Nedergaard, J. (2004). Brown adipose tissue: function and physiological significance. Physiol Rev, 84(1), 277-359. doi:10.1152/physrev.00015.2003

59. Morak, M., Schmidinger, H., Riesenhuber, G., Rechberger, G. N., Kollroser, M., Haemmerle, G., . . . Hermetter, A. (2012). Adipose triglyceride lipase (ATGL) and hormone-sensitive lipase (HSL) deficiencies affect expression of lipolytic activities in mouse adipose tissues. Mol Cell Proteomics, 11(12), 1777-1789. doi:10.1074/mcp.M111.015743

60. Busiello, R. A., Savarese, S., & Lombardi, A. (2015). Mitochondrial uncoupling proteins and energy metabolism. Front Physiol, 6, 36. doi:10.3389/fphys.2015.00036

61. Huh, J. Y., Panagiotou, G., Mougios, V., Brinkoetter, M., Vamvini, M. T., Schneider, B. E., & Mantzoros, C. S. (2012). FNDC5 and irisin in humans: I. Predictors of circulating concentrations in serum and plasma and II. mRNA expression and circulating concentrations in response to weight loss and exercise. Metabolism, 61(12), 1725-1738. doi: 10.1016/j.metabol.2012.09.002

62. Roca-Rivada, A., Castelao, C., Senin, L. L., Landrove, M. O., Baltar, J., Belén Crujeiras, A., . . . Pardo, M. (2013). FNDC5/irisin is not only a myokine but also an adipokine. PLoS One, 8(4), e60563. doi:10.1371/journal.pone.0060563

63. Aydin, S., Kuloglu, T., Aydin, S., Kalayci, M., Yilmaz, M., Cakmak, T., . . . Ozercan, I. H. (2014). A comprehensive immunohistochemical examination of the distribution of the fat-burning protein irisin in biological tissues. Peptides, 61, 130-136. doi: 10.1016/j.peptides.2014.09.014

64. Boström, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., . . . Spiegelman, B. M. (2012). A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature, 481(7382), 463-468. doi:10.1038/nature10777

65. Zhang, Y., Li, R., Meng, Y., Li, S., Donelan, W., Zhao, Y., . . . Tang, D. (2014). Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling. Diabetes, 63(2), 514-525. doi:10.2337/db13-1106

66. Chen, Y., Ding, J., Zhao, Y., Ju, S., Mao, H., & Peng, X. G. (2021). Irisin induces white adipose tissue browning in mice as assessed by magnetic resonance imaging. Exp Biol Med (Maywood), 246(14), 1597-1606. doi:10.1177/15353702211006049

67. Luo, Y., Qiao, X., Ma, Y., Deng, H., Xu, C. C., & Xu, L. (2020). Disordered metabolism in mice lacking irisin. Sci Rep, 10(1), 17368. doi:10.1038/s41598-020-74588-7

68. Xiong, Y., Wu, Z., Zhang, B., Wang, C., Mao, F., Liu, X., . . . Kuang, S. (2019). Fndc5 loss-of-function attenuates exercise-induced browning of white adipose tissue in mice. Faseb j, 33(5), 5876-5886. doi:10.1096/fj.201801754RR

69. Xiong, X. Q., Chen, D., Sun, H. J., Ding, L., Wang, J. J., Chen, Q., . . . Zhu, G. Q. (2015). FNDC5 overexpression and irisin ameliorate glucose/lipid metabolic derangements and enhance lipolysis in obesity. Biochim Biophys Acta, 1852(9), 1867-1875. doi: 10.1016/j.bbadis.2015.06.017

70. Gao, S., Li, F., Li, H., Huang, Y., Liu, Y., & Chen, Y. (2016). Effects and Molecular Mechanism of GST-Irisin on Lipolysis and Autocrine Function in 3T3-L1 Adipocytes. PLoS One, 11(1), e0147480. doi: 10.1371/journal.pone.0147480

71. Zhang, Z., Yang, D., Xiang, J., Zhou, J., Cao, H., Che, Q., . . . Su, Z. (2021). Non shivering Thermogenesis Signalin Regulation and Potential Therapeutic Applications of Brown Adipose Tissue. Int J Biol Sci, 17(11), 2853-2870. doi:10.7150/ijbs.60354

72. Carrillo, A. E., & Flouris, A. D. (2011). Caloric restriction and longevity: effects of reduced body temperature. Aging Res Rev, 10(1), 153-162. doi: 10.1016/j.arr.2010.10.001

73. Kajimura, S., & Saito, M. (2014). A new era in brown adipose tissue biology: molecular control of brown fat development and energy homeostasis. Annu Rev Physiol, 76, 225-249. doi:10.1146/annurev-physiol-021113-170252

74. Valente, A., Carrillo, A. E., Tzatzarakis, M. N., Vakonaki, E., Tsatsakis, A. M., Kenny, G. P., . . . Flouris, A. D. (2015). The absorption and metabolism of a single L-menthol oral versus skin administration: Effects on thermogenesis and metabolic rate. Food Chem Toxicol, 86, 262-273. doi: 10.1016/j.fct.2015.09.018

75. Zhang, S., Yang, L., Chen, P., Jin, H., Xie, X., Yang, M., . . . Yu, X. (2016). Circulating Adipocyte Fatty Acid Binding Protein (FABP4) Levels Are Associated with Irisin in the Middle-Aged General Chinese Population. PLoS One, 11(1), e0146605. doi: 10.1371/journal.pone.0146605

76. Ma, E. B., Sahar, N. E., Jeong, M., & Huh, J. Y. (2019). Irisin Exerts Inhibitory Effect on Adipogenesis Through Regulation of Wnt Signaling. Front Physiol, 10, 1085. doi:10.3389/fphys.2019.01085

77. Chmurzyńska, A. (2006). The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet, 47(1), 39-48. doi:10.1007/bf03194597

78. Bag, S., Ramaiah, S., & Anbarasu, A. (2015). fabp4 is central to eight obesity associated genes: a functional gene network-based polymorphic study. J Theor Biol, 364, 344-354. doi:10.1016/j.jtbi.2014.09.034

79. Kim, H. M., Lee, Y. K., Kim, E. S., & Koo, J. S. (2020). Energy transfer from adipocytes to cancer cells in breast cancer. Neoplasma, 67(5), 992-1001. doi:10.4149/neo_2020_191017N1050

80. Prentice, K. J., Saksi, J., & Hotamisligil, G. S. (2019). Adipokine FABP4 integrates energy stores and counterregulatory metabolic responses. J Lipid Res, 60(4), 734-740. doi:10.1194/jlr.S091793

81. Hao, J., Zhang, Y., Yan, X., Yan, F., Sun, Y., Zeng, J., . . . Li, B. (2018). Circulating Adipose Fatty Acid Binding Protein Is a New Link Underlying Obesity-Associated Breast/Mammary Tumor Development. Cell Metab, 28(5), 689-705.e685. doi: 10.1016/j.cmet.2018.07.006

82. Zeng, J., Sauter, E. R., & Li, B. (2020). FABP4: A New Player in Obesity-Associated Breast Cancer. Trends Mol Med, 26(5), 437-440. doi: 10.1016/j.molmed.2020.03.004

83. Bao, P. P., Cai, H., Peng, P., Gu, K., Su, Y., Shu, X. O., & Zheng, Y. (2016). Body mass index and weight change in relation to triple-negative breast cancer survival. Cancer Causes Control, 27(2), 229-236. doi:10.1007/s10552-015-0700-7

84. Cespedes Feliciano, E. M., Kroenke, C. H., Bradshaw, P. T., Chen, W. Y., Prado, C. M., Weltzien, E. K., . . . Caan, B. J. (2017). Postdiagnosis Weight Change and Survival Following a Diagnosis of Early-Stage Breast Cancer. Cancer Epidemiol Biomarkers Prev, 26(1), 44-50. doi:10.1158/1055-9965.Epi-16-0150

85. Shang, L., Hattori, M., Fleming, G., Jaskowiak, N., Hedeker, D., Olopade, O. I., & Huo, D. (2021). Impact of post diagnosis weight change on survival outcomes in Black and White breast cancer patients. Breast Cancer Res, 23(1), 18. doi:10.1186/s13058-021-01397-9

86. Rybinska, I., Agresti, R., Trapani, A., Tagliabue, E., & Triulzi, T. (2020). Adipocytes in Breast Cancer, the Thick and the Thin. Cells, 9(3). doi:10.3390/cells9030560

87. Rybinska, I., Mangano, N., Tagliabue, E., & Triulzi, T. (2021). Cancer-Associated Adipocytes in Breast Cancer: Causes and Consequences. Int J Mol Sci, 22(7). doi:10.3390/ijms22073775

Published
2024-11-14
How to Cite
Zhu, J., Li, C., Tian, S., & Ding, M. (2024). The effects of muscle factors irisin on lipid metabolism in breast cancer: A possible mechanism anti-tumor mechanism of physical activity. Molecular & Cellular Biomechanics, 21(3), 345. https://doi.org/10.62617/mcb345
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