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Therapeutic and immunomodulatory role of probiotics in breast cancer: A mechanistic review

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Abstract

Breast cancer has become the most prevalent and noxious type of malignancy around the globe (Giaquinto et al., 2022). Multiple clinical strategies including chemotherapy, radiotherapy, and immunotherapy have been in practice to manage breast cancer. Besides the protective roles of conventional remedial approaches, and non-reversible and deteriorative impacts like healthy cell damage, organ failure, etc., the world scientific community is in a continuous struggle to find some alternative biocompatible and comparatively safe solutions. Among novel breast cancer management/treatment options, the role of probiotics has become immensely important. The current review encompasses the prevalence statistics of breast cancer across the globe concerning developed and undeveloped counties, intestinal microbiota linkage with breast cancer, and association of breast microbiome with breast carcinoma. Furthermore, this review also narrates the role of probiotics against breast cancer and their mode of action. In Vivo and In Vitro studies under breast cancer research regarding probiotics are mechanistically explained. The current review systematically explains the immunomodulatory role of probiotics to prevent breast cancer. Last, but not the least, current review concludes the use of probiotics in the treatment of breast cancer through various mechanisms and future recommendations for molecular basis studies.

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Data availability

The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abdoli M, Fathi Rezaei P, Mansouri K (2021) Exploring the anticancer efficacy of mixture of local probiotics on MDA-MB-231 and MCF-7 breast cell lines. Journal of Cell and Molecular Research 13(1):54–64

  • Abreu MT, Fukata M, Arditi M (2005) TLR signaling in the gut in health and disease. J Immunol 174(8):4453–4460

    Article  CAS  PubMed  Google Scholar 

  • Albert-Bayo M, Paracuellos I, González-Castro AM, Rodríguez-Urrutia A, Rodríguez-Lagunas MJ, Alonso-Cotoner C et al (2019) Intestinal mucosal mast cells: key modulators of barrier function and homeostasis. Cells 8(2):135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson RC, Cookson AL, McNabb WC, Kelly WJ, Roy NC (2010) Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function. FEMS Microbiology Letters 309(2):184–192

  • Aragón F, Carino S, Perdigón G, de LeBlanc ADM (2014) The administration of milk fermented by the probiotic Lactobacillus casei CRL 431 exerts an immunomodulatory effect against a breast tumour in a mouse model. Immunobiology 219(6):457–464

  • Badgeley A, Anwar H, Modi K, Murphy P, Lakshmikuttyamma A (2021) Effect of probiotics and gut microbiota on anti-cancer drugs: mechanistic perspectives. Biochim Biophys Acta Rev Cancer 1875(1):188494

    Article  CAS  PubMed  Google Scholar 

  • Becker MH, Walke JB, Cikanek S, Savage AE, Mattheus N, Santiago C.N, Gratwicke B (2015) Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus. Proceedings of the Royal Society B: Biological Sciences 282(1805):20142881

  • Bedada TL, Feto TK, Awoke KS, Garedew AD, Yifat FT, Birri DJ (2020) Probiotics for cancer alternative prevention and treatment. Biomed Pharmacother 129:110409

    Article  Google Scholar 

  • Behzadi R, Hormati A, Eivaziatashbeik K, Ahmadpour S, Khodadust F, Zaboli F, Seidi K (2021) Evaluation of anti-tumor potential of Lactobacillus acidophilus ATCC4356 culture supernatants in MCF-7 breast cancer. Anti-Cancer Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry-Anti-Cancer Agents) 21(14):1861–1870

  • Bharti V, Mehta A, Singh S, Jain N, Ahirwal L (2015) Cytotoxicity Of Live Whole Cell, Heat Killed Cell And Cell Free Extract Of Lactobacillus Strain In U-87 Human Glioblastoma Cell Line And Mcf-7 Breast Cancer Cell Line. International Journal of Probiotics & Prebiotics (4)

  • Biffi A, Coradini D, Larsen R, Riva L, Di Fronzo G (1997) Antiproliferative effect of fermented milk on the growth of a human breast cancer cell line. Nutrition and Cancer. 28(1):93-99

  • Blobe GC, Schiemann WP, Lodish HF (2000) Role of transforming growth factor β in human disease. N Engl J Med 342(18):1350–1358

    Article  CAS  PubMed  Google Scholar 

  • Buck BL, Altermann E, Svingerud T, Klaenhammer TR (2005) Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71(12):8344–8351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caballero-Franco C, Keller K, De Simone C, Chadee K (2007) The VSL# 3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol-Gastrointest Liver Physiol 292(1):G315–G322

    Article  CAS  PubMed  Google Scholar 

  • Caminero A, Meisel M, Jabri B, Verdu EF (2019) Mechanisms by which gut microorganisms influence food sensitivities. Nat Rev Gastroenterol Hepatol 16(1):7–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castagliuolo I, Galeazzi F, Ferrari S, Elli M, Brun P, Cavaggioni A et al (2005) Beneficial effect of auto-aggregating Lactobacillus crispatus on experimentally induced colitis in mice. FEMS Immunol Med Microbiol 43(2):197–204

    Article  CAS  PubMed  Google Scholar 

  • Castillo NA, Perdigón G, de Moreno de LeBlanc A (2011) Oral administration of a probiotic Lactobacillus modulates cytokine production and TLR expression improving the immune response against Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol 11:1–12

    Article  Google Scholar 

  • Chen C, Chan HM, Kubow S (2007) Kefir extracts suppress in vitro proliferation of estrogen-dependent human breast cancer cells but not normal mammary epithelial cells. J Med Food 10(3):416–422

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Shen B, Jiang Z (2022) Traditional Chinese medicine prescription Shenling BaiZhu powder to treat ulcerative colitis: clinical evidence and potential mechanisms. Front Pharmacol 13:978558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chenoll E, Casinos B, Bataller E, Astals P, Echevarría J, Iglesias JR et al (2011) Novel probiotic Bifidobacterium bifidum CECT 7366 strain active against the pathogenic bacterium Helicobacter pylori. Appl Environ Microbiol 77(4):1335–1343

    Article  CAS  PubMed  Google Scholar 

  • Choi SS, Kim Y, Han KS, You S, Oh S, Kim SH (2006) Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Letters in Applied Microbiology 42(5):452–458

  • Coconnier MH, Bernet MF, Chauvière G, Servin AL (1993) Adhering heat-killed human Lactobacillus acidophilus, strain LB, inhibits the process of pathogenicity of diarrhoeagenic bacteria in cultured human intestinal cells. J Diarrhoeal Dis Res 11(4):235–242

    CAS  PubMed  Google Scholar 

  • Collado MC, Gueimonde M, Hernandez M, Sanz Y, Salminen S (2005) Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. J Food Prot 68(12):2672–2678

    Article  PubMed  Google Scholar 

  • Dallal MMS, Mokarrari S, Yazdi MH, Mohtasab TPA, Shirazi L, Mahdavi M (2012a) Modulatory effects of Lactobacillus reuteri on cellular immune parameters in mice breast adenocarcinoma. Tehran Univ Med J 70(1):1–6

    Google Scholar 

  • Dallal MMS, Yazdi MH, Holakuyee M, Hassan ZM, Abolhassani M, Mahdavi M (2012b) Lactobacillus casei ssp. casei induced Th1 cytokine profile and natural killer cells activity in invasive ductal carcinoma bearing mice. Iran J Allergy Asthma Immunol 11(2): 183–189

  • De Leblanc ADM, Matar C, Perdigón G (2007) The application of probiotics in cancer. British Journal of Nutrition 98(S1):S105–S110

  • De Leblanc ADM, Matar C, Thériault C, Perdigón G (2005) Effects of milk fermented by Lactobacillus helveticus R389 on immune cells associated to mammary glands in normal and a breast cancer model. Immunobiology 210(5):349–358

  • De Keersmaecker SC, Verhoeven TL, Desair J, Marchal K, Vanderleyden J, Nagy I (2006) Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiol Lett 259(1):89–96

    Article  PubMed  Google Scholar 

  • de La Cruz-Merino L, Chiesa M, Caballero R, Rojo F, Palazón N, Carrasco FH, Sánchez-Margalet V (2017) Breast cancer immunology and immunotherapy: current status and future perspectives. Int Rev Cell Mol Biol 331:1–53

    Article  PubMed  Google Scholar 

  • Denkova R, Goranov B, Teneva D, Denkova Z, Kostov G (2017) Antimicrobial activity of probiotic microorganisms: mechanisms of interaction and methods of examination. In: Méndez-Vilas A (ed) Antimicrobial research: novel bioknowledge and educational programs, Fomatex Research Centre S.L., 1st edn. p 102–112

  • Deo SVS, Sharma J, Kumar S (2022) GLOBOCAN 2020 report on global cancer burden: challenges and opportunities for surgical oncologists. Ann Surg Oncol 29(11):6497–6500

    Article  CAS  PubMed  Google Scholar 

  • DeSantis CE, Ma J, Gaudet MM, Newman LA, Miller KD, Goding Sauer A et al (2019) Breast cancer statistics, 2019. CA Cancer J Clin 69(6):438–451

    Article  PubMed  Google Scholar 

  • Dong TS, Gupta A (2019) Influence of early life, diet, and the environment on the microbiome. Clin Gastroenterol Hepatol 17(2):231–242

    Article  PubMed  Google Scholar 

  • Dong H, Rowland I, Tuohy KM, Thomas LV, Yaqoob P (2010) Selective effects of Lactobacillus casei Shirota on T cell activation, natural killer cell activity and cytokine production. Clin Exp Immunol 161(2):378–388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Atti SA, Wasicek K, Mark S, Hegazi R (2009) Use of probiotics in the management of chemotherapy-induced diarrhea: a case study. J Parenter Enter Nutr 33(5):569–570

    Article  Google Scholar 

  • Erdman SE, Poutahidis T (2015) Gut bacteria and cancer. Biochim Biophys Acta Rev Cancer 1856(1):86–90

    Article  CAS  Google Scholar 

  • Fong FLY, Shah NP, Kirjavainen P, El-Nezami H (2016) Mechanism of action of probiotic bacteria on intestinal and systemic immunities and antigen-presenting cells. Int Rev Immunol 35(3):179–188

    Article  CAS  PubMed  Google Scholar 

  • Gallo RL, Hooper LV (2012) Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 12(7):503–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garnier L, Valence F, Mounier J (2017) Diversity and control of spoilage fungi in dairy products: an update. Microorganisms 5(3):42

    Article  PubMed  PubMed Central  Google Scholar 

  • Georgieva M, Georgiev K, Dobromirov P (2015) Probiotics and immunity. In: Immunopathology and immunomodulation. IntechOpen

  • Ghadimi D, Vrese MD, Heller KJ, Schrezenmeir J (2010) Effect of natural commensal-origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integrity of polarized intestinal epithelial cells. Inflamm Bowel Dis 16(3):410–427

    Article  PubMed  Google Scholar 

  • Ghafouri-Fard S, Shamsi R, Seifi-Alan M, Javaheri M, Tabarestani S (2014) Cancer–testis genes as candidates for immunotherapy in breast cancer. Immunotherapy 6(2):165–179

  • Giaquinto AN, Sung H, Miller KD, Kramer JL, Newman LA, Minihan A et al (2022) Breast cancer statistics, 2022. CA Cancer J Clin 72(6):524–541

    Article  PubMed  Google Scholar 

  • Gonzalez-Angulo AM, Timms KM, Liu S, Chen H, Litton JK, Potter J et al (2011) Incidence and outcome of BRCA mutations in unselected patients with triple receptor-negative breast cancer. Clin Cancer Res 17(5):1082–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gopal PK, Prasad J, Smart J, Gill HS (2001) In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int J Food Microbiol 67(3):207–216

    Article  CAS  PubMed  Google Scholar 

  • Han KJ, Lee NK, Park H, Paik HD (2015) Anticancer and anti-inflammatory activity of probiotic Lactococcus lactis NK34. Journal of microbiology and biotechnology 25(10):1697–1701

  • Hassan Z, Mustafa S, Rahim RA, Isa NM (2016) Anti-breast cancer effects of live, heat-killed and cytoplasmic fractions of Enterococcus faecalis and Staphylococcus hominis isolated from human breast milk. In Vitro Cell Dev Biol-Anim 52(3):337–348

    Article  PubMed  Google Scholar 

  • Heer E, Harper A, Escandor N, Sung H, McCormack V, Fidler-Benaoudia MM (2020) Global burden and trends in premenopausal and postmenopausal breast cancer: a population-based study. Lancet Glob Health 8(8):e1027–e1037

    Article  PubMed  Google Scholar 

  • Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H et al (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408(6813):740–745

    Article  CAS  PubMed  Google Scholar 

  • Imani Fooladi AA, Hossein Yazdi M, Pourmand MR, Mirshafiey A, Hassan ZM, Azizi T et al (2015) Th1 cytokine production induced by Lactobacillus acidophilus in BALB/c mice bearing transplanted breast tumor. Jundishapur J Microbiol 8(4):e17354

    Article  PubMed  PubMed Central  Google Scholar 

  • Iyer C, Kosters A, Sethi G, Kunnumakkara AB, Aggarwal BB, Versalovic J (2008) Probiotic Lactobacillus reuteri promotes TNF‐induced apoptosis in human myeloid leukemia‐derived cells by modulation of NF‐κB and MAPK signalling. Cellular microbiology 10(7):1442–1452

  • Kadidrareddy RH, Mathakala VANI, Palempalli UD (2016) Therapeutic activity of conjugated linoleic acids synthesized by Lactobacillus plantarum. Int J Pharm Bio Sci 7(4):215–223

    Article  CAS  Google Scholar 

  • Kaga C, Takagi A, Kano M, Kado S, Kato I, Sakai M, Toi M (2013) L actobacillus casei S hirota enhances the preventive efficacy of soymilk in chemically induced breast cancer. Cancer science 104(11):1508–1514

  • Kassayova M, Bobrov N, Strojný L, Orendáš P, Demečková V, Jendželovský R, Fedoročko P (2016) Anticancer and immunomodulatory effects of Lactobacillus plantarum LS/07, inulin and melatonin in NMU-induced rat model of breast cancer. Anticancer research 36(6):2719–2728

  • Khare A, Thorat G, Bhimte A, Yadav V (2018) Mechanism of action of prebiotic and probiotic. immunity 3:27–27

  • Kieser KJ, Kagan JC (2017) Multi-receptor detection of individual bacterial products by the innate immune system. Nat Rev Immunol 17(6):376–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12(5):319–330

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim PI, Jung MY, Chang YH, Kim S, Kim SJ, Park YH (2007) Probiotic properties of Lactobacillus and Bifidobacterium strains isolated from porcine gastrointestinal tract. Applied microbiology and biotechnology 74:1103–1111

  • Kinjo Y, Wu D, Kim G, Xing GW, Poles MA, Ho DD et al (2005) Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434(7032):520–525

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Kumar A, Nagpal R, Mohania D, Behare P, Verma V et al (2010) Cancer-preventing attributes of probiotics: an update. Int J Food Sci Nutr 61(5):473–496

    Article  CAS  PubMed  Google Scholar 

  • Lee NK, Han KJ, Son SH, Eom SJ, Lee SK, Paik HD (2015) Multifunctional effect of probiotic Lactococcus lactis KC24 isolated from kimchi. LWT-Food Sci Technol 64(2):1036–1041

    Article  CAS  Google Scholar 

  • Lee NK, Son SH, Jeon EB, Jung GH, Lee JY, Paik HD (2015) The prophylactic effect of probiotic Bacillus polyfermenticus KU3 against cancer cells. Journal of functional foods 14:513–518

  • Li D, Wu M (2011) Pattern recognition receptors in health and diseases. Signal Transduct Target Ther 6(1):291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu CF, Hu CL, Chiang SS, Tseng KC, Yu RC, Pan TM (2009) Beneficial preventive effects of gastric mucosal lesion for soy− skim milk fermented by lactic acid bacteria. J Agric Food Chem 57(10):4433–4438

    Article  CAS  PubMed  Google Scholar 

  • Lucero-Prisno DE III, Shomuyiwa DO, Kouwenhoven MBN, Dorji T, Odey GO, Miranda AV et al (2023) Top 10 public health challenges to track in 2023: shifting focus beyond a global pandemic. Public Health Chall 2(2):e86

    Article  Google Scholar 

  • Makras L, Triantafyllou V, Fayol-Messaoudi D, Adriany T, Zoumpopoulou G, Tsakalidou E et al (2006) Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Res Microbiol 157(3):241–247

    Article  CAS  PubMed  Google Scholar 

  • Malik SS, Saeed A, Baig M, Asif N, Masood N, Yasmin A (2018) Anticarcinogenecity of microbiota and probiotics in breast cancer. Int J Food Prop 21(1):655–666

    Article  CAS  Google Scholar 

  • Markowiak P, Śliżewska K (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9(9):1021

    Article  PubMed  PubMed Central  Google Scholar 

  • Maroof H, Hassan ZM, Mobarez AM, Mohamadabadi MA (2015) Lactobacillus acidophilus could modulate the immune response against breast cancer in murine model. J Clin Immunol 32:1353–1359

  • Mauch A, Dal Bello F, Coffey A, Arendt EK (2010) The use of Lactobacillus brevis PS1 to in vitro inhibit the outgrowth of Fusarium culmorum and other common Fusarium species found on barley. Int J Food Microbiol 141(1–2):116–121

    Article  CAS  PubMed  Google Scholar 

  • McQuade RM, Stojanovska V, Abalo R, Bornstein JC, Nurgali K (2016) Chemotherapy-induced constipation and diarrhea: pathophysiology, current and emerging treatments. Front Pharmacol 7:414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menyhárt O, Fekete JT, Győrffy B (2018) Demographic shift disproportionately increases cancer burden in an aging nation: current and expected incidence and mortality in Hungary up to 2030. Clin Epidemiol 10:1093–1108

    Article  PubMed  PubMed Central  Google Scholar 

  • Momenimovahed Z, Salehiniya H (2019) Epidemiological characteristics of and risk factors for breast cancer in the world. Breast Cancer Targets Ther 11:151

    Article  Google Scholar 

  • Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A (2019) Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl Microbiol Biotechnol 103(16):6463–6472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moradi M, Kousheh SA, Almasi H, Alizadeh A, Guimarães JT, Yılmaz N, Lotfi A (2020) Postbiotics produced by lactic acid bacteria: the next frontier in food safety. Compr Rev Food Sci Food Saf 19(6):3390–3415

    Article  PubMed  Google Scholar 

  • Müller CA, Autenrieth IB, Peschel A (2005) Innate defenses of the intestinal epithelial barrier. Cell Mol Life Sci CMLS 62(12):1297–1307

    Article  PubMed  Google Scholar 

  • Nami Y, Haghshenas B, Haghshenas M, Abdullah N, Yari Khosroushahi A (2015) The prophylactic effect of probiotic Enterococcus lactis IW5 against different human cancer cells. Front Microbiol 6:1317

    Article  PubMed  PubMed Central  Google Scholar 

  • Oelschlaeger TA (2010) Mechanisms of probiotic actions–a review. Int J Med Microbiol 300(1):57–62

    Article  CAS  PubMed  Google Scholar 

  • Ohland CL, MacNaughton WK (2010) Probiotic bacteria and intestinal epithelial barrier function. American journal of physiology-gastrointestinal and liver physiology 298(6):G807–G819

  • O’Shea EF, Cotter PD, Stanton C, Ross RP, Hill C (2012) Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol 152(3):189–205

    Article  CAS  PubMed  Google Scholar 

  • Ouwehand AC, Salminen S, Tölkkö S, Roberts P, Ovaska J, Salminen E (2002) Resected human colonic tissue: new model for characterizing adhesion of lactic acid bacteria. Clin Vaccine Immunol 9(1):184–186

    Article  Google Scholar 

  • Pakbin B, Dibazar SP, Allahyari S, Javadi M, Amani Z, Farasat A, Darzi S (2022) Anticancer properties of probiotic Saccharomyces boulardii supernatant on human breast cancer cells. Probiotics and Antimicrobial Proteins 14(6):1130–1138

  • Perdigon G, Galdeano CM, Valdez JC, Medici M (2002) Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56(4):S21–S26

    Article  CAS  PubMed  Google Scholar 

  • Pogačar MŠ, Langerholc T, Mičetić-Turk D, Možina SS, Klančnik A (2020) Effect of Lactobacillus spp. on adhesion, invasion, and translocation of Campylobacter jejuni in chicken and pig small-intestinal epithelial cell lines. BMC Vet Res 16(1):1–14

    Google Scholar 

  • Pourbaferani M, Modiri S, Norouzy A, Maleki H, Heidari M, Alidoust L, Noghabi KA (2021) A newly characterized potentially probiotic strain, Lactobacillus brevis MK05, and the toxicity effects of its secretory proteins against MCF-7 breast cancer cells. Probiotics and antimicrobial proteins 13:982–992

  • Praharaj I, John SM, Bandyopadhyay R, Kang G (2015) Probiotics, antibiotics and the immune responses to vaccines. Philos Trans R Soc B Biol Sci 370(1671):20140144

    Article  Google Scholar 

  • Rajagopala SV, Vashee S, Oldfield LM, Suzuki Y, Venter JC, Telenti A, Nelson KE (2017) The human microbiome and cancer. Cancer Prev Res 10(4):226–234

    Article  Google Scholar 

  • Reid G, Sanders ME, Gaskins HR, Gibson GR, Mercenier A, Rastall R et al (2003) New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol 37(2):105–118

    Article  PubMed  Google Scholar 

  • Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl J-P, Ricciardi-Castagnoli P (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2:361–367

    Article  CAS  PubMed  Google Scholar 

  • Ruo SW, Alkayyali T, Win M, Tara A, Joseph C, Kannan A et al (2021) Role of gut microbiota dysbiosis in breast cancer and novel approaches in prevention, diagnosis, and treatment. Cureus 13(8):e17472

    PubMed  PubMed Central  Google Scholar 

  • Saber A, Alipour B, Faghfoori Z, Yari Khosroushahi A (2017) Cellular and molecular effects of yeast probiotics on cancer. Crit Rev Microbiol 43(1):96–115

    Article  PubMed  Google Scholar 

  • Sánchez B, Delgado S, Blanco-Míguez A, Lourenço A, Gueimonde M, Margolles A (2017) Probiotics, gut microbiota, and their influence on host health and disease. Mol Nutr Food Res 61(1):1600240

    Article  Google Scholar 

  • Sarkarsi R, Elias SMS, Lee SP (2023) The experience of patients with breast cancer at home during chemotherapy treatment: a qualitative approach. Int J Care Sch 6(1):47–58

    Article  Google Scholar 

  • Schuijt TJ, van der Poll T, de Vos WM, Wiersinga WJ (2013) The intestinal microbiota and host immune interactions in the critically ill. Trends Microbiol 21(5):221–229

    Article  CAS  PubMed  Google Scholar 

  • Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13(11):800–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shida K, Kiyoshima-Shibata J, Kaji R, Nagaoka M, Nanno M (2009) Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology 128:e858–e869

    Article  PubMed  PubMed Central  Google Scholar 

  • Shojaei F, Zhong C, Wu X, Yu L, Ferrara N (2008) Role of myeloid cells in tumor angiogenesis and growth. Trends Cell Biol 18(8):372–378

    Article  CAS  PubMed  Google Scholar 

  • Siegel RL, Miller KD, Wagle NS, Jemal A (2023) Cancer statistics, 2023. Ca Cancer J Clin 73(1):17–48

    Article  PubMed  Google Scholar 

  • Silva EO, de Carvalho TC, Parshikov IA, dos Santos RA, Emery FS, Furtado NJC (2014) Cytotoxicity of lapachol metabolites produced by probiotics. Lett Appl Microbiol 59(1):108–114

    Article  CAS  Google Scholar 

  • Singh KS, Kumar S, Mohanty AK, Grover S, Kaushik JK (2018) Mechanistic insights into the host-microbe interaction and pathogen exclusion mediated by the Mucus-binding protein of Lactobacillus plantarum. Sci Rep 8(1):1–10

    Article  Google Scholar 

  • Singh R, Zogg H, Wei L, Bartlett A, Ghoshal UC, Rajender S, Ro S (2021) Gut microbial dysbiosis in the pathogenesis of gastrointestinal dysmotility and metabolic disorders. J Neurogastroenterol Motil 27(1):19

    Article  PubMed  PubMed Central  Google Scholar 

  • Soltan Dallal MM, Yazdi MH, Hassan ZM, Holakuyee M, Abedi Mohtasab TP, Aminharaty F et al (2010) Effect of oral administration of Lactobacillus acidophilus on the immune responses and survival of BALB/c mice bearing human breast cancer. Tehran Univ Med J 67(11):753–758

    Google Scholar 

  • Standish LJ, Dowd F, Sweet E, Dale L, Andersen MR (2018) Do women with breast cancer who choose adjunctive integrative oncology care receive different standard oncologic treatment?. Integr Cancer Ther 17(3):874–884

  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249

    Article  PubMed  Google Scholar 

  • Tharakan S, Zhong X, Galsky MD (2021) The impact of the globalization of cancer clinical trials on the enrollment of Black patients. Cancer 127(13):2294–2301

    Article  PubMed  Google Scholar 

  • Tooley KL, Howarth GS, Lymn KA, Lawrence A, Butler RN (2006) Oral ingestion of Streptococcus thermophilus diminishes severity of small intestinal mucositis in methotrexate treated rats. Cancer Biol Ther 5(6):593–600

    Article  CAS  PubMed  Google Scholar 

  • Tooley KL, Howarth GS, Lymn KA, Lawrence A, Butler RN (2011) Oral ingestion of Streptococcus thermophilus does not affect mucositis severity or tumor progression in the tumor-bearing rat. Cancer Biol Ther 12(2):131–138

    Article  CAS  PubMed  Google Scholar 

  • Toumazi D, El Daccache S, Constantinou C (2021) An unexpected link: the role of mammary and gut microbiota on breast cancer development and management. Oncol Rep 45(5):1–15

    Article  Google Scholar 

  • Upadhaya P, Kharkar P, Patil A, Pawar S, Disouza J, Patravale VB (2021) Probiotics and cancer: boosting the immune system. Probiotic research in therapeutics. Springer, Singapore, pp 47–67

    Chapter  Google Scholar 

  • Urbaniak C, Gloor GB, Brackstone M, Scott L, Tangney M, Reid G (2016) The microbiota of breast tissue and its association with breast cancer. Appl Environ Microbiol 82(16):5039–5048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Zyl WF, Deane SM, Dicks LM (2020) Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria. Gut Microbes 12(1):1831339

    Article  PubMed  PubMed Central  Google Scholar 

  • Vélez MP, De Keersmaecker SC, Vanderleyden J (2007) Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol Lett 276(2):140–148

    Article  PubMed  Google Scholar 

  • Wan MLY, Forsythe SJ, El-Nezami H (2019) Probiotics interaction with foodborne pathogens: a potential alternative to antibiotics and future challenges. Crit Rev Food Sci Nutr 59(20):3320–3333

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Feng B, Niu C, Jia S, Sun C, Wang Z et al (2019) Dendritic cell targeting of bovine viral diarrhea virus E2 protein expressed by Lactobacillus casei effectively induces antigen-specific immune responses via oral vaccination. Viruses 11(6):575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wells JM (2011) Immunomodulatory mechanisms of lactobacilli. Microb Cell Fact 10(1):1–15

    Google Scholar 

  • Williams NT (2010) Probiotics. Am J Health-Syst Pharm 67(6):449–458

    Article  CAS  PubMed  Google Scholar 

  • Worah K, Mathan TS, Manh TPV, Keerthikumar S, Schreibelt G, Tel J et al (2016) Proteomics of human dendritic cell subsets reveals subset-specific surface markers and differential inflammasome function. Cell Rep 16(11):2953–2966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu HJ, Wu E (2012) The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3(1):4–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Yazdi MH, Mahdavi M, Kheradmand E, Shahverdi AR (2012) The preventive oral supplementation of a selenium nanoparticle-enriched probiotic increases the immune response and lifespan of 4T1 breast cancer bearing mice. Arzneimittelforschung 62(11):525–531

  • Yazdi MH, Dallal MMS, Hassan ZM, Holakuyee M, Amiri SA, Abolhassani M, Mahdavi M (2010) Oral administration of Lactobacillus acidophilus induces IL-12 production in spleen cell culture of BALB/c mice bearing transplanted breast tumour. Br J Nutr 104(2):227–232

    Article  CAS  PubMed  Google Scholar 

  • Yi D, Kim S (2021) Human breast milk composition and function in human health: from nutritional components to microbiome and microRNAs. Nutrients 13(9):3094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yousefi B, Eslami M, Ghasemian A, Kokhaei P, Salek Farrokhi A, Darabi N (2019) Probiotics importance and their immunomodulatory properties. J Cell Physiol 234(6):8008–8018

    Article  CAS  PubMed  Google Scholar 

  • Yu AQ, Li L (2016) The potential role of probiotics in cancer prevention and treatment. Nutr Cancer 68(4):535–544

    Article  PubMed  Google Scholar 

  • Zamarron BF, Chen W (2011) Dual roles of immune cells and their factors in cancer development and progression. Int J Biol Sci 7(5):651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamberi NR, Abu N, Mohamed NE, Nordin N, Keong YS, Beh BK et al (2016) The antimetastatic and antiangiogenesis effects of kefir water on murine breast cancer cells. Integr Cancer Ther 15(4):NP53–NP66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Tang H, Chen P, Xie H, Tao Y (2019) Demystifying the manipulation of host immunity, metabolism, and extraintestinal tumors by the gut microbiome. Signal Transduct Target Ther 4(1):1–34

    CAS  Google Scholar 

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MS wrote the manuscript. SA planned, supervised, edited the manuscript and analyzed the data. UF wrote the manuscript and pictorial work. MT analyzed the data. MI provided the data for mechanistic study and analyzed the data. SM assisted in writeup. HS assisted in writeup. RM edited the manuscript. RK edited the manuscript. HF assisted in writeup and reference management.

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Correspondence to Shaukat Ali.

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As no animal is being used/sacrificed in present study, ethical approval was not applicable.

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Communicated by Ran Wang.

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Summer, M., Ali, S., Fiaz, U. et al. Therapeutic and immunomodulatory role of probiotics in breast cancer: A mechanistic review. Arch Microbiol 205, 296 (2023). https://doi.org/10.1007/s00203-023-03632-7

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  • DOI: https://doi.org/10.1007/s00203-023-03632-7

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