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Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

Does Gut-breast Microbiota Axis Orchestrates Cancer Progression?

Author(s): Maria Michela Marino, Bianca Maria Nastri, Marina D’Agostino, Rossella Risolo, Alessandra De Angelis, Giuliana Settembre, Monica Rienzo, Vittoria D’Esposito, Ciro Abbondanza, Pietro Formisano, Andrea Ballini*, Luigi Santacroce*, Mariarosaria Boccellino and Marina Di Domenico

Volume 22, Issue 11, 2022

Published on: 04 August, 2022

Page: [1111 - 1122] Pages: 12

DOI: 10.2174/1871530322666220331145816

Price: $65

Abstract

Breast cancer, even today, can cause death. Therefore, prevention and early detection are fundamental factors. The mechanisms that favour it are genetic and epigenetic, and seem to play a significant role; also, the microbiota can change estrogen levels and can induce chronic inflammation in the neoplastic site, alternating the balance between proliferation and cell death. Activated steroid hormone receptors induce transcription of genes that encode for proteins involved in cell proliferation and activate another transduction pathway, inducing cell cycle progression and cell migration. These important studies have allowed to develop therapies with selective modulators of estrogen receptors (SERMs), able to block their proliferative and pro-tumorigenic action. Of fundamental importance is also the role played by the microbiota in regulating the metabolism of estrogens and their levels in the blood. There are microbial populations that are able to promote the development of breast cancer, through the production of enzymes responsible for the deconjugation of estrogens, the increase of these in the intestine, subsequent circulation and migration to other locations, such as the udder. Other microbial populations are, instead, able to synthesize estrogen compounds or mimic estrogenic action, and interfere with the metabolism of drugs, affecting the outcome of therapies. The microbial composition of the intestine and hormonal metabolism depend largely on eating habits; the consumption of fats and proteins favours the increase of estrogen in the blood, unlike a diet rich in fiber. Therefore, in-depth knowledge of the microbiota present in the intestine-breast axis could, in the future, encourage the development of new diagnostic and therapeutic approaches to breast cancers.

Keywords: Selective modulators of estrogen receptors (SERMs), microbiota, breast cancer, estrogen, hormonal metabolism, gutbreast axis.

Graphical Abstract
[1]
Ferlay, J.; Colombet, M.; Soerjomataram, I.; Mathers, C.; Parkin, D.M.; Piñeros, M.; Znaor, A.; Bray, F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int. J. Cancer, 2019, 144(8), 1941-1953.
[http://dx.doi.org/10.1002/ijc.31937] [PMID: 30350310]
[2]
Winters, S.; Martin, C.; Murphy, D.; Shokar, N.K. Breast cancer epidemiology, prevention, and screening. Prog. Mol. Biol. Transl. Sci., 2017, 151, 1-32.
[http://dx.doi.org/10.1016/bs.pmbts.2017.07.002] [PMID: 29096890]
[3]
Stone, T.W.; McPherson, M.; Gail Darlington, L. Obesity and cancer: Existing and new hypotheses for a causal connection. EBioMedicine, 2018, 30, 14-28.
[http://dx.doi.org/10.1016/j.ebiom.2018.02.022] [PMID: 29526577]
[4]
Salvatore, F. The shift of the paradigm between ageing and diseases. Clin. Chem. Lab. Med., 2020, 58(10), 1635-1644.
[http://dx.doi.org/10.1515/cclm-2020-0125] [PMID: 32286241]
[5]
Kolb, R.; Zhang, W. Obesity and breast cancer: A case of inflamed adipose tissue. Cancers (Basel), 2020, 12(6), 1686.
[http://dx.doi.org/10.3390/cancers12061686] [PMID: 32630445]
[6]
Bousquenaud, M.; Fico, F.; Solinas, G.; Rüegg, C.; Santamaria-Martínez, A. Obesity promotes the expansion of metastasis-initiating cells in breast cancer. Breast Cancer Res., 2018, 20(1), 104.
[http://dx.doi.org/10.1186/s13058-018-1029-4] [PMID: 30180888]
[7]
Saberi-Karimian, M.; Katsiki, N.; Caraglia, M.; Boccellino, M.; Majeed, M.; Sahebkar, A. Vascular endothelial growth factor: An important molecular target of curcumin. Crit. Rev. Food Sci. Nutr., 2019, 59(2), 299-312.
[http://dx.doi.org/10.1080/10408398.2017.1366892] [PMID: 28853916]
[8]
Auricchio, F.; Migliaccio, A.; Castoria, G.; Rotondi, A.; Di Domenico, M.; Pagano, M.; Nola, E. Phosphorylation on tyrosine of oestradiol-17 beta receptor in uterus and interaction of oestradiol-17 beta and glucocorticoid receptors with antiphosphotyrosine antibodies. J. Steroid Biochem., 1987, 27(1-3), 245-253.
[http://dx.doi.org/10.1016/0022-4731(87)90316-5] [PMID: 2447388]
[9]
Migliaccio, A.; Di Domenico, M.; Green, S.; de Falco, A.; Kajtaniak, E.L.; Blasi, F.; Chambon, P.; Auricchio, F. Phosphorylation on tyrosine of in vitro synthesized human estrogen receptor activates its hormone binding. Mol. Endocrinol., 1989, 3(7), 1061-1069.
[http://dx.doi.org/10.1210/mend-3-7-1061] [PMID: 2797002]
[10]
Migliaccio, A.; Pagano, M.; De Goeij, C.C.; Di Domenico, M.; Castoria, G.; Sluyser, M.; Auricchio, F. Phosphorylation and estradiol binding of estrogen receptor in hormone-dependent and hormone-independent GR mouse mammary tumors. Int. J. Cancer, 1992, 51(5), 733-739.
[http://dx.doi.org/10.1002/ijc.2910510512] [PMID: 1612782]
[11]
Cicinelli, E.; Ballini, A.; Marinaccio, M.; Poliseno, A.; Coscia, M.F.; Monno, R.; De Vito, D. Microbiological findings in endometrial specimen: Our experience. Arch. Gynecol. Obstet., 2012, 285(5), 1325-1329.
[http://dx.doi.org/10.1007/s00404-011-2138-9] [PMID: 22113463]
[12]
Beato, M.; Herrlich, P.; Schütz, G. Steroid hormone receptors: Many actors in search of a plot. Cell, 1995, 83(6), 851-857.
[http://dx.doi.org/10.1016/0092-8674(95)90201-5] [PMID: 8521509]
[13]
Mangelsdorf, D.J.; Thummel, C.; Beato, M.; Herrlich, P.; Schütz, G.; Umesono, K.; Blumberg, B.; Kastner, P.; Mark, M.; Chambon, P.; Evans, R.M. The nuclear receptor superfamily: The second decade. Cell, 1995, 83(6), 835-839.
[http://dx.doi.org/10.1016/0092-8674(95)90199-X] [PMID: 8521507]
[14]
Chauhan, S.; Kunz, A.; Davis, K.; Roberts, J.; Martin, G.; Demetiou, M.C.; Sroka, T.C.; Cress, A.E.; Roger, L. Androgen control of cell proliferation and cytoskeletal reorganization in human fibrosarcoma cells. J. Biol. Chem., 2004, 279(2), 937-944.
[http://dx.doi.org/10.1074/jbc.M311325200] [PMID: 14576147]
[15]
Blaustein, J.D. Minireview: Neuronal steroid hormone receptors: They’re not just for hormones anymore. Endocrinology, 2004, 145(3), 1075-1081.
[http://dx.doi.org/10.1210/en.2003-1485] [PMID: 14670984]
[16]
Deroo, B.J.; Korach, K.S. Estrogen receptors and human disease. J. Clin. Invest., 2006, 116(3), 561-570.
[http://dx.doi.org/10.1172/JCI27987] [PMID: 16511588]
[17]
Falkenstein, E.; Norman, A.W.; Wehling, M. Mannheim classification of nongenomically initiated (rapid) steroid action(s). J. Clin. Endocrinol. Metab., 2000, 85(5), 2072-2075.
[http://dx.doi.org/10.1210/jcem.85.5.6516] [PMID: 10843198]
[18]
Castoria, G.; Migliaccio, A.; D’Amato, L.; Di Stasio, R.; Ciociola, A.; Lombardi, M.; Bilancio, A.; Di Domenico, M.; de Falco, A.; Auricchio, F. Integrating signals between cAMP and MAPK pathways in breast cancer. Front. Biosci., 2008, 13(13), 1318-1327.
[http://dx.doi.org/10.2741/2764] [PMID: 17981632]
[19]
Feola, A.; Cimini, A.; Migliucci, F.; Iorio, R.; Zuchegna, C.; Rothenberger, R.; Cito, L.; Porcellini, A.; Unteregger, G.; Tombolini, V.; Giordano, A.; Di Domenico, M. The inhibition of p85αPI3KSer83 phosphorylation prevents cell proliferation and invasion in prostate cancer cells. J. Cell. Biochem., 2013, 114(9), 2114-2119.
[http://dx.doi.org/10.1002/jcb.24558] [PMID: 23553770]
[20]
Cosentino, C.; Di Domenico, M.; Porcellini, A.; Cuozzo, C.; De Gregorio, G.; Santillo, M.R.; Agnese, S.; Di Stasio, R.; Feliciello, A.; Migliaccio, A.; Avvedimento, E.V. p85 regulatory subunit of PI3K mediates cAMP-PKA and estrogens biological effects on growth and survival. Oncogene, 2007, 26(14), 2095-2103.
[http://dx.doi.org/10.1038/sj.onc.1210027] [PMID: 17016431]
[21]
Di Domenico, M.; Castoria, G.; Bilancio, A.; Migliaccio, A.; Auricchio, F. Estradiol activation of human colon carcinoma-derived Caco-2 cell growth. Cancer Res., 1996, 56(19), 4516-4521.
[PMID: 8813150]
[22]
Migliaccio, A.; Di Domenico, M.; Castoria, G.; de Falco, A.; Bontempo, P.; Nola, E.; Auricchio, F. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J., 1996, 15(6), 1292-1300.
[http://dx.doi.org/10.1002/j.1460-2075.1996.tb00471.x] [PMID: 8635462]
[23]
Clemons, M.; Goss, P. Estrogen and the risk of breast cancer. N. Engl. J. Med., 2001, 344(4), 276-285.
[http://dx.doi.org/10.1056/NEJM200101253440407] [PMID: 11172156]
[24]
Yue, W.; Wang, J.P.; Li, Y.; Bocchinfuso, W.P.; Korach, K.S.; Devanesan, P.D.; Rogan, E.; Cavalieri, E.; Santen, R.J. Tamoxifen versus aromatase inhibitors for breast cancer prevention. Clin. Cancer Res., 2005, 11(2 Pt 2), 925s-930s.
[PMID: 15701888]
[25]
Xu, J.; Li, Q. Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol. Endocrinol., 2003, 17(9), 1681-1692.
[http://dx.doi.org/10.1210/me.2003-0116] [PMID: 12805412]
[26]
Liao, L.; Kuang, S.Q.; Yuan, Y.; Gonzalez, S.M.; O’Malley, B.W.; Xu, J. Molecular structure and biological function of the cancer-amplified nuclear receptor coactivator SRC-3/AIB1. J. Steroid Biochem. Mol. Biol., 2002, 83(1-5), 3-14.
[http://dx.doi.org/10.1016/S0960-0760(02)00254-6] [PMID: 12650696]
[27]
Peto, R. Cancer, genes, and the environment. N. Engl. J. Med., 2000, 343(20), 1495.
[PMID: 11184465]
[28]
Love, R.R.; Mazess, R.B.; Barden, H.S.; Epstein, S.; Newcomb, P.A.; Jordan, V.C.; Carbone, P.P.; DeMets, D.L. Effects of tamoxifen on bone mineral density in postmenopausal women with breast cancer. N. Engl. J. Med., 1992, 326(13), 852-856.
[http://dx.doi.org/10.1056/NEJM199203263261302] [PMID: 1542321]
[29]
Katzenellenbogen, J.A.; O’Malley, B.W.; Katzenellenbogen, B.S. Tripartite steroid hormone receptor pharmacology: Interaction with multiple effector sites as a basis for the cell- and promoter-specific action of these hormones. Mol. Endocrinol., 1996, 10(2), 119-131.
[PMID: 8825552]
[30]
Borgna, J.L.; Rochefort, H. High-affinity binding to the estrogen receptor of [3H]4-hydroxytamoxifen, an active antiestrogen metabolite. Mol. Cell. Endocrinol., 1980, 20(1), 71-85.
[http://dx.doi.org/10.1016/0303-7207(80)90095-7] [PMID: 7439523]
[31]
Gradishar, W.; Glusman, J.; Lu, Y.; Vogel, C.; Cohen, F.J.; Sledge, G.W.J., Jr Effects of high dose raloxifene in selected patients with advanced breast carcinoma. Cancer, 2000, 88(9), 2047-2053.
[http://dx.doi.org/10.1002/(SICI)1097-0142(20000501)88:9<2047:AID-CNCR10>3.0.CO;2-E] [PMID: 10813716]
[32]
Delmas, P.D.; Bjarnason, N.H.; Mitlak, B.H.; Ravoux, A.C.; Shah, A.S.; Huster, W.J.; Draper, M.; Christiansen, C. Effects of raloxifene on bone mineral density, serum cholesterol concentrations, and uterine endometrium in postmenopausal women. N. Engl. J. Med., 1997, 337(23), 1641-1647.
[http://dx.doi.org/10.1056/NEJM199712043372301] [PMID: 9385122]
[33]
Goldstein, S.R.; Scheele, W.H.; Rajagopalan, S.K.; Wilkie, J.L.; Walsh, B.W.; Parsons, A.K.A. A 12-month comparative study of raloxifene, estrogen, and placebo on the postmenopausal endometrium. Obstet. Gynecol., 2000, 95(1), 95-103.
[PMID: 10636510]
[34]
Davies, G.C.; Huster, W.J.; Lu, Y.; Plouffe, L., Jr; Lakshmanan, M. Adverse events reported by postmenopausal women in controlled trials with raloxifene. Obstet. Gynecol., 1999, 93(4), 558-565.
[PMID: 10214833]
[35]
Wakeling, A.E.; Bowler, J. Steroidal pure antioestrogens. J. Endocrinol., 1987, 112(3), R7-R10.
[http://dx.doi.org/10.1677/joe.0.112R007] [PMID: 3559447]
[36]
Wakeling, A.E.; Dukes, M.; Bowler, J. A potent specific pure antiestrogen with clinical potential. Cancer Res., 1991, 51(15), 3867-3873.
[PMID: 1855205]
[37]
Lovreglio, P.; Bukvic, N.; Fustinoni, S.; Ballini, A.; Drago, I.; Foà, V.; Guanti, G.; Soleo, L. Lack of genotoxic effect in workers exposed to very low doses of 1,3-butadiene. Arch. Toxicol., 2006, 80(6), 378-381.
[http://dx.doi.org/10.1007/s00204-005-0046-0] [PMID: 16307232]
[38]
Shakespeare, W.; Yang, M.; Bohacek, R.; Cerasoli, F.; Stebbins, K.; Sundaramoorthi, R.; Azimioara, M.; Vu, C.; Pradeepan, S.; Metcalf, C., III; Haraldson, C.; Merry, T.; Dalgarno, D.; Narula, S.; Hatada, M.; Lu, X.; van Schravendijk, M.R.; Adams, S.; Violette, S.; Smith, J.; Guan, W.; Bartlett, C.; Herson, J.; Iuliucci, J.; Weigele, M.; Sawyer, T. Structure-based design of an osteoclast-selective, nonpeptide src homology 2 inhibitor with in vivo antiresorptive activity. Proc. Natl. Acad. Sci. USA, 2000, 97(17), 9373-9378.
[http://dx.doi.org/10.1073/pnas.97.17.9373] [PMID: 10944210]
[39]
Ballini, A.; Scacco, S.; Boccellino, M.; Santacroce, L.; Arrigoni, R. Microbiota and obesity: Where are we now? Biology, 2020, 9(12), 415.
[40]
Grice, E.A.; Kong, H.H.; Conlan, S.; Deming, C.B.; Davis, J.; Young, A.C.; Bouffard, G.G.; Blakesley, R.W.; Murray, P.R.; Green, E.D.; Turner, M.L.; Segre, J.A. NISC Comparative Sequencing Program. Topographical and temporal diversity of the human skin microbiome. Science, 2009, 324(5931), 1190-1192.
[http://dx.doi.org/10.1126/science.1171700] [PMID: 19478181]
[41]
González, A.; Vázquez-Baeza, Y.; Knight, R. SnapShot: The human microbiome. Cell, 2014, 158(3), 690-690.e1.
[http://dx.doi.org/10.1016/j.cell.2014.07.019] [PMID: 25083877]
[42]
Arumugam, M.; Raes, J.; Pelletier, E.; Le Paslier, D.; Yamada, T.; Mende, D.R.; Fernandes, G.R.; Tap, J.; Bruls, T.; Batto, J.M.; Bertalan, M.; Borruel, N.; Casellas, F.; Fernandez, L.; Gautier, L.; Hansen, T.; Hattori, M.; Hayashi, T.; Kleerebezem, M.; Kurokawa, K.; Leclerc, M.; Levenez, F.; Manichanh, C.; Nielsen, H.B.; Nielsen, T.; Pons, N.; Poulain, J.; Qin, J.; Sicheritz-Ponten, T.; Tims, S.; Torrents, D.; Ugarte, E.; Zoetendal, E.G.; Wang, J.; Guarner, F.; Pedersen, O.; de Vos, W.M.; Brunak, S.; Doré, J.; Antolín, M.; Artiguenave, F.; Blottiere, H.M.; Almeida, M.; Brechot, C.; Cara, C.; Chervaux, C.; Cultrone, A.; Delorme, C.; Denariaz, G.; Dervyn, R.; Foerstner, K.U.; Friss, C.; van de Guchte, M.; Guedon, E.; Haimet, F.; Huber, W.; van Hylckama-Vlieg, J.; Jamet, A.; Juste, C.; Kaci, G.; Knol, J.; Lakhdari, O.; Layec, S.; Le Roux, K.; Maguin, E.; Mérieux, A.; Melo Minardi, R.; M’rini, C.; Muller, J.; Oozeer, R.; Parkhill, J.; Renault, P.; Rescigno, M.; Sanchez, N.; Sunagawa, S.; Torrejon, A.; Turner, K.; Vandemeulebrouck, G.; Varela, E.; Winogradsky, Y.; Zeller, G.; Weissenbach, J.; Ehrlich, S.D.; Bork, P. MetaHIT Consortium. Enterotypes of the human gut microbiome. Nature, 2011, 473(7346), 174-180.
[http://dx.doi.org/10.1038/nature09944] [PMID: 21508958]
[43]
Flint, H.J.; Scott, K.P.; Duncan, S.H.; Louis, P.; Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes, 2012, 3(4), 289-306.
[http://dx.doi.org/10.4161/gmic.19897] [PMID: 22572875]
[44]
Qin, J.; Li, R.; Raes, J.; Arumugam, M.; Burgdorf, K.S.; Manichanh, C.; Nielsen, T.; Pons, N.; Levenez, F.; Yamada, T.; Mende, D.R.; Li, J.; Xu, J.; Li, S.; Li, D.; Cao, J.; Wang, B.; Liang, H.; Zheng, H.; Xie, Y.; Tap, J.; Lepage, P.; Bertalan, M.; Batto, J.M.; Hansen, T.; Le Paslier, D.; Linneberg, A.; Nielsen, H.B.; Pelletier, E.; Renault, P.; Sicheritz-Ponten, T.; Turner, K.; Zhu, H.; Yu, C.; Li, S.; Jian, M.; Zhou, Y.; Li, Y.; Zhang, X.; Li, S.; Qin, N.; Yang, H.; Wang, J.; Brunak, S.; Doré, J.; Guarner, F.; Kristiansen, K.; Pedersen, O.; Parkhill, J.; Weissenbach, J.; Bork, P.; Ehrlich, S.D.; Wang, J. MetaHIT Consortium. A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 2010, 464(7285), 59-65.
[http://dx.doi.org/10.1038/nature08821] [PMID: 20203603]
[45]
Gajer, P.; Brotman, R.M.; Bai, G.; Sakamoto, J.; Schütte, U.M.; Zhong, X.; Koenig, S.S.; Fu, L.; Ma, Z.S.; Zhou, X.; Abdo, Z.; Forney, L.J.; Ravel, J. Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med., 2012, 4(132), 132ra52.
[http://dx.doi.org/10.1126/scitranslmed.3003605] [PMID: 22553250]
[46]
David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; Biddinger, S.B.; Dutton, R.J.; Turnbaugh, P.J. Diet rapidly and reproducibly alters the human gut microbiome. Nature, 2014, 505(7484), 559-563.
[http://dx.doi.org/10.1038/nature12820] [PMID: 24336217]
[47]
Wu, G.D.; Chen, J.; Hoffmann, C.; Bittinger, K.; Chen, Y.Y.; Keilbaugh, S.A.; Bewtra, M.; Knights, D.; Walters, W.A.; Knight, R.; Sinha, R.; Gilroy, E.; Gupta, K.; Baldassano, R.; Nessel, L.; Li, H.; Bushman, F.D.; Lewis, J.D. Linking long-term dietary patterns with gut microbial enterotypes. Science, 2011, 334(6052), 105-108.
[http://dx.doi.org/10.1126/science.1208344] [PMID: 21885731]
[48]
Koren, O.; Goodrich, J.K.; Cullender, T.C.; Spor, A.; Laitinen, K.; Bäckhed, H.K.; Gonzalez, A.; Werner, J.J.; Angenent, L.T.; Knight, R.; Bäckhed, F.; Isolauri, E.; Salminen, S.; Ley, R.E. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell, 2012, 150(3), 470-480.
[http://dx.doi.org/10.1016/j.cell.2012.07.008] [PMID: 22863002]
[49]
Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; Heath, A.C.; Warner, B.; Reeder, J.; Kuczynski, J.; Caporaso, J.G.; Lozupone, C.A.; Lauber, C.; Clemente, J.C.; Knights, D.; Knight, R.; Gordon, J.I. Human gut microbiome viewed across age and geography. Nature, 2012, 486(7402), 222-227.
[http://dx.doi.org/10.1038/nature11053] [PMID: 22699611]
[50]
Pérez-Cobas, A.E.; Gosalbes, M.J.; Friedrichs, A.; Knecht, H.; Artacho, A.; Eismann, K.; Otto, W.; Rojo, D.; Bargiela, R.; von Bergen, M.; Neulinger, S.C.; Däumer, C.; Heinsen, F.A.; Latorre, A.; Barbas, C.; Seifert, J.; dos Santos, V.M.; Ott, S.J.; Ferrer, M.; Moya, A. Gut microbiota disturbance during antibiotic therapy: A multiomic approach. Gut, 2013, 62(11), 1591-1601.
[http://dx.doi.org/10.1136/gutjnl-2012-303184] [PMID: 23236009]
[51]
Isacco, C.G.; Ballini, A.; De Vito, D.; Nguyen, K.C.D.; Cantore, S.; Bottalico, L.; Quagliuolo, L.; Boccellino, M.; Di Domenico, M.; Santacroce, L.; Arrigoni, R.; Dipalma, G.; Inchingolo, F. Rebalance the oral microbiota as efficacy tool in endocrine, metabolic, and immune disorders. Endocr. Metab. Immune Disord. Drug Targets, 2020.
[52]
D’Argenio, V.; Salvatore, F. The role of the gut microbiome in the healthy adult status. Clin. Chim. Acta, 2015, 451(Pt A), 97-102.
[http://dx.doi.org/10.1016/j.cca.2015.01.003] [PMID: 25584460]
[53]
Ballini, A.; Dipalma, G.; Isacco, C.G.; Boccellino, M.; Di Domenico, M.; Santacroce, L.; Nguyễn, K.C.D.; Scacco, S.; Calvani, M.; Boddi, A.; Corcioli, F.; Quagliuolo, L.; Cantore, S.; Martelli, F.S.; Inchingolo, F. Oral microbiota and immune system crosstalk: A translational research. Biology (Basel), 2020, 9(6), 131.
[http://dx.doi.org/10.3390/biology9060131] [PMID: 32560235]
[54]
Hunt, K.M.; Foster, J.A.; Forney, L.J.; Schütte, U.M.; Beck, D.L.; Abdo, Z.; Fox, L.K.; Williams, J.E.; McGuire, M.K.; McGuire, M.A. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One, 2011, 6(6), e21313.
[http://dx.doi.org/10.1371/journal.pone.0021313] [PMID: 21695057]
[55]
Shapira, I.; Sultan, K.; Lee, A.; Taioli, E. Evolving concepts: How diet and the intestinal microbiome act as modulators of breast malignancy. ISRN Oncol., 2013, 2013, 693920.
[http://dx.doi.org/10.1155/2013/693920] [PMID: 24187630]
[56]
Marteau, P. Bacterial flora in inflammatory bowel disease. Dig. Dis., 2009, 27(Suppl. 1), 99-103.
[http://dx.doi.org/10.1159/000268128] [PMID: 20203504]
[57]
Shreiner, A.B.; Kao, J.Y.; Young, V.B. The gut microbiome in health and in disease. Curr. Opin. Gastroenterol., 2015, 31(1), 69-75.
[http://dx.doi.org/10.1097/MOG.0000000000000139] [PMID: 25394236]
[58]
Jurjus, A.; Eid, A.; Al Kattar, S.; Zeenny, M.N.; Gerges-Geagea, A.; Haydar, H.; Hilal, A.; Oueidat, D.; Matar, M.; Tawilah, J.; Hussein, I.H.; Schembri-Wismayer, P.; Cappello, F.; Tomasello, G.; Leone, A.; Jurjus, R.A. Inflammatory bowel disease, colorectal cancer and type 2 diabetes mellitus: The links. BBA Clin., 2015, 5, 16-24.
[http://dx.doi.org/10.1016/j.bbacli.2015.11.002] [PMID: 27051585]
[59]
Bhatt, A.P.; Redinbo, M.R.; Bultman, S.J. The role of the microbiome in cancer development and therapy. CA Cancer J. Clin., 2017, 67(4), 326-344.
[http://dx.doi.org/10.3322/caac.21398] [PMID: 28481406]
[60]
Crocetto, F.; Boccellino, M.; Barone, B.; Di Zazzo, E.; Sciarra, A.; Galasso, G.; Settembre, G.; Quagliuolo, L.; Imbimbo, C.; Boffo, S.; Angelillo, I.F.; Di Domenico, M. The crosstalk between prostate cancer and microbiota inflammation: Nutraceutical products are useful to balance this interplay? Nutrients, 2020, 12(9), 2648.
[http://dx.doi.org/10.3390/nu12092648] [PMID: 32878054]
[61]
Garrido-Navas, C.; de Miguel-Perez, D.; Exposito-Hernandez, J.; Bayarri, C.; Amezcua, V.; Ortigosa, A.; Valdivia, J.; Guerrero, R.; Garcia Puche, J.L.; Lorente, J.A.; Serrano, M.J. Cooperative and escaping mechanisms between circulating tumor cells and blood constituents. Cells, 2019, 8(11), 1382.
[http://dx.doi.org/10.3390/cells8111382] [PMID: 31684193]
[62]
Mikó, E.; Kovács, T.; Sebő, É.; Tóth, J.; Csonka, T.; Ujlaki, G.; Sipos, A.; Szabó, J.; Méhes, G.; Bai, P. Microbiome-microbial metabolome-cancer cell interactions in breast cancer-familiar, but unexplored. Cells, 2019, 8(4), 293.
[http://dx.doi.org/10.3390/cells8040293] [PMID: 30934972]
[63]
Rea, D.; Coppola, G.; Palma, G.; Barbieri, A.; Luciano, A.; Del Prete, P.; Rossetti, S.; Berretta, M.; Facchini, G.; Perdonà, S.; Turco, M.C.; Arra, C. Microbiota effects on cancer: From risks to therapies. Oncotarget, 2018, 9(25), 17915-17927.
[http://dx.doi.org/10.18632/oncotarget.24681] [PMID: 29707157]
[64]
Hieken, T.J.; Chen, J.; Hoskin, T.L.; Walther-Antonio, M.; Johnson, S.; Ramaker, S.; Xiao, J.; Radisky, D.C.; Knutson, K.L.; Kalari, K.R.; Yao, J.Z.; Baddour, L.M.; Chia, N.; Degnim, A.C. The microbiome of aseptically collected human breast tissue in benign and malignant disease. Sci. Rep., 2016, 6(1), 30751.
[http://dx.doi.org/10.1038/srep30751] [PMID: 27485780]
[65]
Laborda-Illanes, A.; Sanchez-Alcoholado, L.; Dominguez-Recio, M.E.; Jimenez-Rodriguez, B.; Lavado, R.; Comino-Méndez, I.; Alba, E.; Queipo-Ortuño, M.I. Breast and gut microbiota action mechanisms in breast cancer pathogenesis and treatment. Cancers (Basel), 2020, 12(9), 2465.
[http://dx.doi.org/10.3390/cancers12092465] [PMID: 32878124]
[66]
Urbaniak, C.; Gloor, G.B.; Brackstone, M.; Scott, L.; Tangney, M.; Reid, G. The microbiota of breast tissue and its association with breast cancer. Appl. Environ. Microbiol., 2016, 82(16), 5039-5048.
[http://dx.doi.org/10.1128/AEM.01235-16] [PMID: 27342554]
[67]
Flores, R.; Shi, J.; Gail, M.H.; Gajer, P.; Ravel, J.; Goedert, J.J. Association of fecal microbial diversity and taxonomy with selected enzymatic functions. PLoS One, 2012, 7(6), e39745.
[http://dx.doi.org/10.1371/journal.pone.0039745] [PMID: 22761886]
[68]
Plottel, C.S.; Blaser, M.J. Microbiome and malignancy. Cell Host Microbe, 2011, 10(4), 324-335.
[http://dx.doi.org/10.1016/j.chom.2011.10.003] [PMID: 22018233]
[69]
Fuhrman, B.J.; Feigelson, H.S.; Flores, R.; Gail, M.H.; Xu, X.; Ravel, J.; Goedert, J.J. Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women. J. Clin. Endocrinol. Metab., 2014, 99(12), 4632-4640.
[http://dx.doi.org/10.1210/jc.2014-2222] [PMID: 25211668]
[70]
Fernández, M.F.; Reina-Pérez, I.; Astorga, J.M.; Rodríguez-Carrillo, A.; Plaza-Díaz, J.; Fontana, L. Breast cancer and its relationship with the microbiota. Int. J. Environ. Res. Public Health, 2018, 15(8), 1747.
[http://dx.doi.org/10.3390/ijerph15081747] [PMID: 30110974]
[71]
Ballini, A.; Cantore, S.; Fatone, L.; Montenegro, V.; De Vito, D.; Pettini, F.; Crincoli, V.; Antelmi, A.; Romita, P.; Rapone, B.; Miniello, G.; Perillo, L.; Grassi, F.R.; Foti, C. Transmission of nonviral sexually transmitted infections and oral sex. J. Sex. Med., 2012, 9(2), 372-384.
[http://dx.doi.org/10.1111/j.1743-6109.2011.02515.x] [PMID: 22023797]
[72]
Flores, R.; Shi, J.; Fuhrman, B.; Xu, X.; Veenstra, T.D.; Gail, M.H.; Gajer, P.; Ravel, J.; Goedert, J.J. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: A cross-sectional study. J. Transl. Med., 2012, 10(1), 253.
[http://dx.doi.org/10.1186/1479-5876-10-253] [PMID: 23259758]
[73]
Yang, J.; Tan, Q.; Fu, Q.; Zhou, Y.; Hu, Y.; Tang, S.; Zhou, Y.; Zhang, J.; Qiu, J.; Lv, Q. Gastrointestinal microbiome and breast cancer: Correlations, mechanisms and potential clinical implications. Breast Cancer, 2017, 24(2), 220-228.
[http://dx.doi.org/10.1007/s12282-016-0734-z] [PMID: 27709424]
[74]
Kwa, M.; Plottel, C.S.; Blaser, M.J.; Adams, S. The intestinal microbiome and estrogen receptor-positive female breast cancer. J. Natl. Cancer Inst., 2016, 108(8), djw029.
[PMID: 27107051]
[75]
Holder, G.; Makin, H.L.J.; Bradlow, H.L. The Measurement of Estrogens.Steroid Analysis; Makin, H.L.J; Gower, D.B., Eds.; Springer: Dordrecht, The Netherlands, 2010, Vol. 1, pp. 605-742.
[http://dx.doi.org/10.1023/b135931_8]
[76]
Kisiela, M.; Skarka, A.; Ebert, B.; Maser, E. Hydroxysteroid dehydrogenases (HSDs) in bacteria: A bioinformatic perspective. J. Steroid Biochem. Mol. Biol., 2012, 129(1-2), 31-46.
[http://dx.doi.org/10.1016/j.jsbmb.2011.08.002] [PMID: 21884790]
[77]
Schwabe, R.F.; Jobin, C. The microbiome and cancer. Nat. Rev. Cancer, 2013, 13(11), 800-812.
[http://dx.doi.org/10.1038/nrc3610] [PMID: 24132111]
[78]
Carrega, P.; Bonaccorsi, I.; Di Carlo, E.; Morandi, B.; Paul, P.; Rizzello, V.; Cipollone, G.; Navarra, G.; Mingari, M.C.; Moretta, L.; Ferlazzo, G. CD56(bright)perforin(low) noncytotoxic human NK cells are abundant in both healthy and neoplastic solid tissues and recirculate to secondary lymphoid organs via afferent lymph. J. Immunol., 2014, 192(8), 3805-3815.
[http://dx.doi.org/10.4049/jimmunol.1301889] [PMID: 24646734]
[79]
Delgado, S.; Arroyo, R.; Jiménez, E.; Marín, M.L.; del Campo, R.; Fernández, L.; Rodríguez, J.M. Staphylococcus epidermidis strains isolated from breast milk of women suffering infectious mastitis: Potential virulence traits and resistance to antibiotics. BMC Microbiol., 2009, 9(1), 82.
[http://dx.doi.org/10.1186/1471-2180-9-82] [PMID: 19422689]
[80]
Delgado, S.; García, P.; Fernández, L.; Jiménez, E.; Rodríguez-Baños, M.; del Campo, R.; Rodríguez, J.M. Characterization of staphylococcus aureus strains involved in human and bovine mastitis. FEMS Immunol. Med. Microbiol., 2011, 62(2), 225-235.
[http://dx.doi.org/10.1111/j.1574-695X.2011.00806.x] [PMID: 21477005]
[81]
Heikkilä, M.P.; Saris, P.E.J. Inhibition of staphylococcus aureus by the commensal bacteria of human milk. J. Appl. Microbiol., 2003, 95(3), 471-478.
[http://dx.doi.org/10.1046/j.1365-2672.2003.02002.x] [PMID: 12911694]
[82]
Martín, R.; Langa, S.; Reviriego, C.; Jimínez, E.; Marín, M.L.; Xaus, J.; Fernández, L.; Rodríguez, J.M. Human milk is a source of lactic acid bacteria for the infant gut. J. Pediatr., 2003, 143(6), 754-758.
[http://dx.doi.org/10.1016/j.jpeds.2003.09.028] [PMID: 14657823]
[83]
Kovács, T.; Mikó, E.; Ujlaki, G.; Sári, Z.; Bai, P. The microbiome as a component of the tumor microenvironment. Adv. Exp. Med. Biol., 2020, 1225, 137-153.
[http://dx.doi.org/10.1007/978-3-030-35727-6_10] [PMID: 32030653]
[84]
Smith, P.M.; Howitt, M.R.; Panikov, N.; Michaud, M.; Gallini, C.A.; Bohlooly-Y, M.; Glickman, J.N.; Garrett, W.S. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science, 2013, 341(6145), 569-573.
[http://dx.doi.org/10.1126/science.1241165] [PMID: 23828891]
[85]
Wong, S.H.; Yu, J. Gut microbiota in colorectal cancer: Mechanisms of action and clinical applications. Nat. Rev. Gastroenterol. Hepatol., 2019, 16(11), 690-704.
[http://dx.doi.org/10.1038/s41575-019-0209-8] [PMID: 31554963]
[86]
Charitos, I.A.; Ballini, A.; Cantore, S.; Boccellino, M.; Di Domenico, M.; Borsani, E.; Nocini, R.; Di Cosola, M.; Santacroce, L.; Bottalico, L. Stem cells: A historical review about biological, religious, and ethical issues. Stem Cells Int., 2021, 2021(29), 9978837.
[http://dx.doi.org/10.1155/2021/9978837] [PMID: 34012469]
[87]
Savas, P.; Salgado, R.; Denkert, C.; Sotiriou, C.; Darcy, P.K.; Smyth, M.J.; Loi, S. Clinical relevance of host immunity in breast cancer: From TILs to the clinic. Nat. Rev. Clin. Oncol., 2016, 13(4), 228-241.
[http://dx.doi.org/10.1038/nrclinonc.2015.215] [PMID: 26667975]
[88]
Chin, S.F.; Liu, W.; Storkson, J.M.; Ha, Y.L.; Pariza, M.W. Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J. Food Compos. Anal., 1992, 5(3), 185-197.
[http://dx.doi.org/10.1016/0889-1575(92)90037-K]
[89]
Liu, S.; Foulkes, W.D.; Leung, S.; Gao, D.; Lau, S.; Kos, Z.; Nielsen, T.O. Prognostic significance of FOXP3+ tumor-infiltrating lymphocytes in breast cancer depends on estrogen receptor and human epidermal growth factor receptor-2 expression status and concurrent cytotoxic T-cell infiltration. Breast Cancer Res., 2014, 16(5), 432.
[http://dx.doi.org/10.1186/s13058-014-0432-8] [PMID: 25193543]
[90]
Gupta, R.; Babb, J.S.; Singh, B.; Chiriboga, L.; Liebes, L.; Adams, S.; Demaria, S. The numbers of FoxP3+ lymphocytes in sentinel lymph nodes of breast cancer patients correlate with primary tumor size but not nodal status. Cancer Invest., 2011, 29(6), 419-425.
[http://dx.doi.org/10.3109/07357907.2011.585193] [PMID: 21649468]
[91]
Curiel, T.J.; Coukos, G.; Zou, L.; Alvarez, X.; Cheng, P.; Mottram, P.; Evdemon-Hogan, M.; Conejo-Garcia, J.R.; Zhang, L.; Burow, M.; Zhu, Y.; Wei, S.; Kryczek, I.; Daniel, B.; Gordon, A.; Myers, L.; Lackner, A.; Disis, M.L.; Knutson, K.L.; Chen, L.; Zou, W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med., 2004, 10(9), 942-949.
[http://dx.doi.org/10.1038/nm1093] [PMID: 15322536]
[92]
DeNardo, D.G.; Coussens, L.M. Inflammation and breast cancer. Balancing immune response: Crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res., 2007, 9(4), 212.
[http://dx.doi.org/10.1186/bcr1746] [PMID: 17705880]
[93]
Slack, E.; Hapfelmeier, S.; Stecher, B.; Velykoredko, Y.; Stoel, M.; Lawson, M.A.; Geuking, M.B.; Beutler, B.; Tedder, T.F.; Hardt, W.D.; Bercik, P.; Verdu, E.F.; McCoy, K.D.; Macpherson, A.J. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science, 2009, 325(5940), 617-620.
[http://dx.doi.org/10.1126/science.1172747] [PMID: 19644121]
[94]
Moor, K.; Diard, M.; Sellin, M.E.; Felmy, B.; Wotzka, S.Y.; Toska, A.; Bakkeren, E.; Arnoldini, M.; Bansept, F.; Co, A.D.; Völler, T.; Minola, A.; Fernandez-Rodriguez, B.; Agatic, G.; Barbieri, S.; Piccoli, L.; Casiraghi, C.; Corti, D.; Lanzavecchia, A.; Regoes, R.R.; Loverdo, C.; Stocker, R.; Brumley, D.R.; Hardt, W.D.; Slack, E. High-avidity IgA protects the intestine by enchaining growing bacteria. Nature, 2017, 544(7651), 498-502.
[http://dx.doi.org/10.1038/nature22058] [PMID: 28405025]
[95]
Wu, W.; Sun, M.; Chen, F.; Cao, A.T.; Liu, H.; Zhao, Y.; Huang, X.; Xiao, Y.; Yao, S.; Zhao, Q.; Liu, Z.; Cong, Y. Microbiota metabolite short-chain fatty acid acetate promotes intestinal IgA response to microbiota which is mediated by GPR43. Mucosal Immunol., 2017, 10(4), 946-956.
[http://dx.doi.org/10.1038/mi.2016.114] [PMID: 27966553]
[96]
Goedert, J.J.; Hua, X.; Bielecka, A.; Okayasu, I.; Milne, G.L.; Jones, G.S.; Fujiwara, M.; Sinha, R.; Wan, Y.; Xu, X.; Ravel, J.; Shi, J.; Palm, N.W.; Feigelson, H.S. Postmenopausal breast cancer and oestrogen associations with the IgA-coated and IgA-noncoated faecal microbiota. Br. J. Cancer, 2018, 118(4), 471-479.
[http://dx.doi.org/10.1038/bjc.2017.435] [PMID: 29360814]
[97]
Di Benedetto, A.; Posa, F.; Carbone, C.; Cantore, S.; Brunetti, G.; Centonze, M.; Grano, M.; Lo Muzio, L.; Cavalcanti-Adam, E.A.; Mori, G. NURR1 Downregulation favors osteoblastic differentiation of MSCs. Stem Cells Int., 2017, 2017, 7617048.
[http://dx.doi.org/10.1155/2017/7617048] [PMID: 28769982]
[98]
Wang, H.; Altemus, J.; Niazi, F.; Green, H.; Calhoun, B.C.; Sturgis, C.; Grobmyer, S.R.; Eng, C. Breast tissue, oral and urinary microbiomes in breast cancer. Oncotarget, 2017, 8(50), 88122-88138.
[http://dx.doi.org/10.18632/oncotarget.21490] [PMID: 29152146]
[99]
Boccellino, M.; Di Stasio, D.; Dipalma, G.; Cantore, S.; Ambrosio, P.; Coppola, M.; Quagliuolo, L.; Scarano, A.; Malcangi, G.; Borsani, E.; Rinaldi, B.; Nuzzolese, M.; Xhajanka, E.; Ballini, A.; Inchingolo, F.; Di Domenico, M. Steroids and growth factors in oral squamous cell carcinoma: Useful source of dental-derived stem cells to develop a steroidogenic model in new clinical strategies. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(20), 8730-8740.
[PMID: 31696459]
[100]
Oh, S.; Oh, C.; Yoo, K.H.; Duvall, K.; Sieling, P.A.; Pieber, T.R.; Vaishampayan, P.A.; Love, S.M.; Sumin, O. Functional roles of CTCF in breast cancer. BMB Rep., 2017, 50(9), 445-453.
[http://dx.doi.org/10.5483/BMBRep.2017.50.9.108] [PMID: 28648147]
[101]
Begović, J.; Jovčić, B.; Papić-Obradović, M.; Veljović, K.; Lukić, J.; Kojić, M.; Topisirović, L. Genotypic diversity and virulent factors of Staphylococcus epidermidis isolated from human breast milk. Microbiol. Res., 2013, 168(2), 77-83.
[http://dx.doi.org/10.1016/j.micres.2012.09.004] [PMID: 23098640]
[102]
Chan, A.A.; Bashir, M.; Rivas, M.N.; Duvall, K.; Sieling, P.A.; Pieber, T.R.; Vaishampayan, P.A.; Love, S.M.; Lee, D.J. Characterization of the microbiome of nipple aspirate fluid of breast cancer survivors. Sci. Rep., 2016, 6(1), 28061.
[http://dx.doi.org/10.1038/srep28061] [PMID: 27324944]
[103]
Jeffery, I.B.; O’Toole, P.W. Diet-microbiota interactions and their implications for healthy living. Nutrients, 2013, 5(1), 234-252.
[http://dx.doi.org/10.3390/nu5010234] [PMID: 23344252]
[104]
Feng, Y.; Spezia, M.; Huang, S.; Yuan, C.; Zeng, Z.; Zhang, L.; Ji, X.; Liu, W.; Huang, B.; Luo, W.; Liu, B.; Lei, Y.; Du, S.; Vuppalapati, A.; Luu, H.H.; Haydon, R.C.; He, T.C.; Ren, G. Breast cancer development and progression: Risk factors, cancer stem cells, signaling pathways, genomics, and molecular pathogenesis. Genes Dis., 2018, 5(2), 77-106.
[http://dx.doi.org/10.1016/j.gendis.2018.05.001] [PMID: 30258937]
[105]
Wang, C.; Bai, F.; Zhang, L.H.; Scott, A.; Li, E.; Pei, X.H. Estrogen promotes estrogen receptor negative BRCA1-deficient tumor initiation and progression. Breast Cancer Res., 2018, 20(1), 74.
[http://dx.doi.org/10.1186/s13058-018-0996-9] [PMID: 29996906]

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