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Cited by 27Microbial Metabolites in Food BiotechnologyGut microbiota and healthProbiotics and Fermented Foods

Dietary Supplementation of Inulin Contributes to the Prevention of Estrogen Receptor-Negative Mammary Cancer by Alteration of Gut Microbial Communities and Epigenetic Regulations

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Wu, Huixin, Van Der Pol, William J., Dubois, Laura G., Morrow, Casey D., Tollefsbol, Trygve O.·2023·International Journal of Molecular Sciences
DOI 10.3390/ijms24109015PMC PMC10218871
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Abstract

Breast cancer (BC) is among the most frequently diagnosed malignant cancers in women in the United States. Diet and nutrition supplementation are closely related to BC onset and progression, and inulin is commercially available as a health supplement to improve gut health. However, little is known with respect to inulin intake for BC prevention. We investigated the effect of an inulin-supplemented diet on the prevention of estrogen receptor-negative mammary carcinoma in a transgenic mouse model. Plasma short-chain fatty acids were measured, the gut microbial composition was analyzed, and the expression of proteins related to cell cycle and epigenetics-related genes was measured. Inulin supplementation greatly inhibited tumor growth and significantly delayed tumor latency. The mice that consumed inulin had a distinct microbiome and higher diversity of gut microbial composition compared to the control. The concentration of propionic acid in plasma was significantly higher in the inulin-supplemented group. The protein expression of epigenetic-modulating histone deacetylase 2 (Hdac2), Hdac8, and DNA methyltransferase 3b decreased. The protein expression of factors related to tumor cell proliferation and survival, such as Akt, phospho-PI3K, and NF-kB, also decreased with inulin administration. Furthermore, sodium propionate showed BC prevention effect in vivo through epigenetic regulations. These studies suggest that modulating microbial composition through inulin consumption may be a promising strategy for BC prevention.

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  • Inulin diet resulted in a decrease in expression of proteins pivotal to tumor cell proliferation and survival, such as Akt, phospho-PI3K, and NF-kB.

    “Concurrently, there was a discernible decrease in the expression of proteins pivotal to tumor cell proliferation and survival, such as Akt, phospho-PI3K, and NF-kB.”

    From Drug repurposing for cancer therapy (2024) · cites this paper as [225]

    Results §2.4 reports decreased phospho-PI3K and NF-κB p65 protein expression in inulin-supplemented groups. Although Methods §4.4 lists an Akt antibody, the Results and Discussion do not report a decrease in Akt expression, so that part of the claim is unsupported. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • In a study by Wu et al., rodents fed an inulin-enriched diet exhibited a markedly diverse and robust gut microbiome compared to their counterparts.

    “In a landmark study by Wu et al., rodents fed an inulin-enriched diet exhibited a markedly diverse and robust gut microbiome compared to their counterparts.”

    From Drug repurposing for cancer therapy (2024) · cites this paper as [225]

    Results §2.2.1 reports greater gut microbial diversity in inulin-fed mice than in controls before tumor onset, particularly in the 15% inulin group. The claim omits that timing: Results §2.2.2 says alpha diversity was not significantly different from controls after tumors developed. The paper reports increased beneficial bacteria in the 15% group, but does not establish a generally more ‘robust’ microbiome throughout the study. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Inclusion of inulin in the diet resulted in a significant increase in plasma propionate levels and a decline in expression of HDAC2, HDAC8, and DNA methyltransferase 3b.

    “The inclusion of inulin in the diet resulted in a significant increase in plasma propionate levels and a concomitant decline in the expression of pivotal epigenetic regulatory proteins such as HDAC2, HDAC8, and DNA methyltransferase 3b.”

    From Drug repurposing for cancer therapy (2024) · cites this paper as [225]

  • Dietary inulin has potential as a preventative tactic against breast cancer, potentially leveraging epigenetic mechanisms.

    “This study highlights the potential of dietary inulin as an avant-garde tactic in the preventative arsenal against breast cancer, potentially leveraging epigenetic mechanisms to manifest its prophylactic effects.225”

    From Drug repurposing for cancer therapy (2024) · cites this paper as [225]

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  1. [1]Lukasiewicz S. Czeczelewski M. Forma A. Baj J. Sitarz R. Stanislawek A. Breast Cancer-Epidemiology, Risk Factors, Classification, Prognostic Markers, and Current Treatment Strategies-An Updated Review Cancers 2021 13 4287 10.3390/cancers13174287 34503097 PMC8428369 · DOI
  2. [2]Li S. Chen M. Li Y. Tollefsbol T.O. Prenatal epigenetics diets play protective roles against environmental pollution Clin. Epigenetics 2019 11 82 10.1186/s13148-019-0659-4 31097039 PMC6524340 · DOI
  3. [3]Chen J.Q. Russo J. ERalpha-negative and triple negative breast cancer: Molecular features and potential therapeutic approaches Biochim. Biophys. Acta 2009 1796 162 175 10.1016/j.bbcan.2009.06.003 19527773 PMC2937358 · DOI
  4. [4]Rozeboom B. Dey N. De P. ER+ metastatic breast cancer: Past, present, and a prescription for an apoptosis-targeted future Am. J. Cancer Res. 2019 9 2821 2831 31911865 PMC6943351
  5. [5]Fadnes L.T. Okland J.M. Haaland O.A. Johansson K.A. Correction: Estimating impact of food choices on life expectancy: A modeling study PLoS Med. 2022 19 e1003962 10.1371/journal.pmed.1003962 35333861 PMC8956181 · DOI
  6. [6]Farvid M.S. Spence N.D. Holmes M.D. Barnett J.B. Fiber consumption and breast cancer incidence: A systematic review and meta-analysis of prospective studies Cancer 2020 126 3061 3075 10.1002/cncr.32816 32249416 · DOI
  7. [7]Jaye K. Chang D. Li C.G. Bhuyan D.J. Gut Metabolites and Breast Cancer: The Continuum of Dysbiosis, Breast Cancer Risk, and Potential Breast Cancer Therapy Int. J. Mol. Sci. 2022 23 9490 10.3390/ijms23169490 36012771 PMC9409206 · DOI
  8. [8]Rastogi Y.R. Saini A.K. Thakur V.K. Saini R.V. New Insights into Molecular Links Between Microbiota and Gastrointestinal Cancers: A Literature Review Int. J. Mol. Sci. 2020 21 3212 10.3390/ijms21093212 32370077 PMC7246717 · DOI
  9. [9]Kashyap S. Pal S. Chandan G. Saini V. Chakrabarti S. Saini N.K. Mittal A. Thakur V.K. Saini A.K. Saini R.V. Understanding the cross-talk between human microbiota and gastrointestinal cancer for developing potential diagnostic and prognostic biomarkers Semin. Cancer Biol. 2022 86 643 651 10.1016/j.semcancer.2021.04.020 33971261 · DOI
  10. [10]Zhang J. Xia Y. Sun J. Breast and gut microbiome in health and cancer Genes Dis. 2021 8 581 589 10.1016/j.gendis.2020.08.002 34291130 PMC8278537 · DOI
  11. [11]van Loo J. Coussement P. de Leenheer L. Hoebregs H. Smits G. On the presence of inulin and oligofructose as natural ingredients in the western diet Crit. Rev. Food Sci. Nutr. 1995 35 525 552 10.1080/10408399509527714 8777017 · DOI
  12. [12]Cronin P. Joyce S.A. O’Toole P.W. O’Connor E.M. Dietary Fibre Modulates the Gut Microbiota Nutrients 2021 13 1655 10.3390/nu13051655 34068353 PMC8153313 · DOI · Paper page
  13. [13]Schwiertz A. Hold G.L. Duncan S.H. Gruhl B. Collins M.D. Lawson P.A. Flint H.J. Blaut M. Anaerostipes caccae gen. nov., sp. nov., a new saccharolytic, acetate-utilising, butyrate-producing bacterium from human faeces Syst. Appl. Microbiol. 2002 25 46 51 10.1078/0723-2020-00096 12086188 · DOI
  14. [14]Duncan S.H. Hold G.L. Barcenilla A. Stewart C.S. Flint H.J. Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces Int. J. Syst. Evol. Microbiol. 2002 52 1615 1620 10.1099/00207713-52-5-1615 12361264 · DOI
  15. [15]Eslami S.Z. Majidzadeh A.K. Halvaei S. Babapirali F. Esmaeili R. Microbiome and Breast Cancer: New Role for an Ancient Population Front. Oncol. 2020 10 120 10.3389/fonc.2020.00120 32117767 PMC7028701 · DOI · Paper page
  16. [16]Wu H. Ganguly S. Tollefsbol T.O. Modulating Microbiota as a New Strategy for Breast Cancer Prevention and Treatment Microorganisms 2022 10 1727 10.3390/microorganisms10091727 36144329 PMC9503838 · DOI
  17. [17]Hoffman J.D. Yanckello L.M. Chlipala G. Hammond T.C. McCulloch S.D. Parikh I. Sun S. Morganti J.M. Green S.J. Lin A.L. Dietary inulin alters the gut microbiome, enhances systemic metabolism and reduces neuroinflammation in an APOE4 mouse model PLoS ONE 2019 14 e0221828 10.1371/journal.pone.0221828 31461505 PMC6713395 · DOI
  18. [18]Li Y. Elmen L. Segota I. Xian Y. Tinoco R. Feng Y. Fujita Y. Segura Munoz R.R. Schmaltz R. Bradley L.M. Prebiotic-Induced Anti-tumor Immunity Attenuates Tumor Growth Cell Rep. 2020 30 1753 1766.e6 10.1016/j.celrep.2020.01.035 32049008 PMC7053418 · DOI · Paper page
  19. [19]Li S. Chen M. Wu H. Li Y. Tollefsbol T.O. Maternal Epigenetic Regulation Contributes to Prevention of Estrogen Receptor-negative Mammary Cancer with Broccoli Sprout Consumption Cancer Prev. Res. 2020 13 449 462 10.1158/1940-6207.CAPR-19-0491 PMC7203003 32184225 · DOI
  20. [20]Sharma M. Li Y. Stoll M.L. Tollefsbol T.O. The Epigenetic Connection Between the Gut Microbiome in Obesity and Diabetes Front. Genet. 2019 10 1329 10.3389/fgene.2019.01329 32010189 PMC6974692 · DOI
  21. [21]Oh S. Ko J.Y. Oh C. Yoo K.H. Targeting the Epigenome as a Novel Therapeutic Approach for Breast Cancer Adv. Exp. Med. Biol. 2017 1026 287 313 10.1007/978-981-10-6020-5_14 29282690 · DOI
  22. [22]Rahman M.M. Brane A.C. Tollefsbol T.O. MicroRNAs and Epigenetics Strategies to Reverse Breast Cancer Cells 2019 8 1214 10.3390/cells8101214 31597272 PMC6829616 · DOI
  23. [23]Ruo S.W. Alkayyali T. Win M. Tara A. Joseph C. Kannan A. Srivastava K. Ochuba O. Sandhu J.K. Went T.R. Role of Gut Microbiota Dysbiosis in Breast Cancer and Novel Approaches in Prevention, Diagnosis, and Treatment Cureus 2021 13 e17472 10.7759/cureus.17472 34513524 PMC8405251 · DOI
  24. [24]Subramani R. Poudel S. Smith K.D. Estrada A. Lakshmanaswamy R. Metabolomics of Breast Cancer: A Review Metabolites 2022 12 643 10.3390/metabo12070643 35888767 PMC9325024 · DOI
  25. [25]Hiam-Galvez K.J. Allen B.M. Spitzer M.H. Systemic immunity in cancer Nat. Rev. Cancer 2021 21 345 359 10.1038/s41568-021-00347-z 33837297 PMC8034277 · DOI · Paper page
  26. [26]Hou M.F. Ou-Yang F. Li C.L. Chen F.M. Chuang C.H. Kan J.Y. Wu C.C. Shih S.L. Shiau J.P. Kao L.C. Comprehensive profiles and diagnostic value of menopausal-specific gut microbiota in premenopausal breast cancer Exp. Mol. Med. 2021 53 1636 1646 10.1038/s12276-021-00686-9 34707191 PMC8569190 · DOI
  27. [27]Mirzaei R. Afaghi A. Babakhani S. Sohrabi M.R. Hosseini-Fard S.R. Babolhavaeji K. Khani Ali Akbari S. Yousefimashouf R. Karampoor S. Role of microbiota-derived short-chain fatty acids in cancer development and prevention Biomed. Pharmacother. 2021 139 111619 10.1016/j.biopha.2021.111619 33906079 · DOI
  28. [28]Disis M.L. Corulli L.R. Gad E.A. Koehnlein M.R. Cecil D.L. Senter P.D. Gardai S.J. Okeley N.M. Therapeutic and Prophylactic Antitumor Activity of an Oral Inhibitor of Fucosylation in Spontaneous Mammary Cancers Mol. Cancer Ther. 2020 19 1102 1109 10.1158/1535-7163.MCT-19-0500 32165557 · DOI
  29. [29]Katayama H. Boldt C. Ladd J.J. Johnson M.M. Chao T. Capello M. Suo J. Mao J. Manson J.E. Prentice R. An Autoimmune Response Signature Associated with the Development of Triple-Negative Breast Cancer Reflects Disease Pathogenesis Cancer Res. 2015 75 3246 3254 10.1158/0008-5472.CAN-15-0248 26088128 PMC4676710 · DOI
  30. [30]Tong L.C. Wang Y. Wang Z.B. Liu W.Y. Sun S. Li L. Su D.F. Zhang L.C. Propionate Ameliorates Dextran Sodium Sulfate-Induced Colitis by Improving Intestinal Barrier Function and Reducing Inflammation and Oxidative Stress Front. Pharmacol. 2016 7 253 10.3389/fphar.2016.00253 27574508 PMC4983549 · DOI
  31. [31]Park H.S. Han J.H. Park J.W. Lee D.H. Jang K.W. Lee M. Heo K.S. Myung C.S. Sodium propionate exerts anticancer effect in mice bearing breast cancer cell xenograft by regulating JAK2/STAT3/ROS/p38 MAPK signaling Acta Pharmacol. Sin. 2021 42 1311 1323 10.1038/s41401-020-00522-2 32973326 PMC8285538 · DOI
  32. [32]Yersal O. Barutca S. Biological subtypes of breast cancer: Prognostic and therapeutic implications World J. Clin. Oncol. 2014 5 412 424 10.5306/wjco.v5.i3.412 25114856 PMC4127612 · DOI
  33. [33]Martinez-Ramirez O.C. Salazar-Pina A. Ceron-Ramirez X. Rubio-Lightbourn J. Torres-Romero F. Casas-Avila L. Castro-Hernandez C. Effect of Inulin Intervention on Metabolic Control and Methylation of INS and IRS1 Genes in Patients with Type 2 Diabetes Mellitus Nutrients 2022 14 5195 10.3390/nu14235195 36501225 PMC9737482 · DOI
  34. [34]Shoaib M. Shehzad A. Omar M. Rakha A. Raza H. Sharif H.R. Shakeel A. Ansari A. Niazi S. Inulin: Properties, health benefits and food applications Carbohydr. Polym. 2016 147 444 454 10.1016/j.carbpol.2016.04.020 27178951 · DOI
  35. [35]Vandeputte D. Falony G. Vieira-Silva S. Wang J. Sailer M. Theis S. Verbeke K. Raes J. Prebiotic inulin-type fructans induce specific changes in the human gut microbiota Gut 2017 66 1968 1974 10.1136/gutjnl-2016-313271 28213610 PMC5739857 · DOI · Paper page
  36. [37]Million M. Lagier J.C. Yahav D. Paul M. Gut bacterial microbiota and obesity Clin. Microbiol. Infect. 2013 19 305 313 10.1111/1469-0691.12172 23452229 · DOI
  37. [38]Parida S. Sharma D. Microbial Alterations and Risk Factors of Breast Cancer: Connections and Mechanistic Insights Cells 2020 9 1091 10.3390/cells9051091 32354130 PMC7290701 · DOI
  38. [39]Yuan T. Wang J. Chen L. Shan J. Di L. Lactobacillus murinus Improved the Bioavailability of Orally Administered Glycyrrhizic Acid in Rats Front. Microbiol. 2020 11 597 10.3389/fmicb.2020.00597 32390962 PMC7193032 · DOI
  39. [40]Hu J. Deng F. Zhao B. Lin Z. Sun Q. Yang X. Wu M. Qiu S. Chen Y. Yan Z. Lactobacillus murinus alleviate intestinal ischemia/reperfusion injury through promoting the release of interleukin-10 from M2 macrophages via Toll-like receptor 2 signaling Microbiome 2022 10 38 10.1186/s40168-022-01227-w 35241180 PMC8896269 · DOI
  40. [41]Liu X. Mao B. Gu J. Wu J. Cui S. Wang G. Zhao J. Zhang H. Chen W. Blautia-a new functional genus with potential probiotic properties? Gut Microbes 2021 13 1 21 10.1080/19490976.2021.1875796 PMC7872077 33525961 · DOI
  41. [42]Maioli T.U. Borras-Nogues E. Torres L. Barbosa S.C. Martins V.D. Langella P. Azevedo V.A. Chatel J.M. Possible Benefits of Faecalibacterium prausnitzii for Obesity-Associated Gut Disorders Front. Pharmacol. 2021 12 740636 10.3389/fphar.2021.740636 34925006 PMC8677946 · DOI
  42. [43]Shi L. Sheng J. Wang M. Luo H. Zhu J. Zhang B. Liu Z. Yang X. Combination Therapy of TGF-beta Blockade and Commensal-derived Probiotics Provides Enhanced Antitumor Immune Response and Tumor Suppression Theranostics 2019 9 4115 4129 10.7150/thno.35131 31281535 PMC6592171 · DOI
  43. [44]Luo Y. Lan C. Li H. Ouyang Q. Kong F. Wu A. Ren Z. Tian G. Cai J. Yu B. Rational consideration of Akkermansia muciniphila targeting intestinal health: Advantages and challenges NPJ Biofilms. Microbiomes 2022 8 81 10.1038/s41522-022-00338-4 36253412 PMC9576740 · DOI
  44. [45]Yeoh Y.K. Sun Y. Ip L.Y.T. Wang L. Chan F.K.L. Miao Y. Ng S.C. Prevotella species in the human gut is primarily comprised of Prevotella copri, Prevotella stercorea and related lineages Sci. Rep. 2022 12 9055 10.1038/s41598-022-12721-4 35641510 PMC9156738 · DOI
  45. [46]Kruse H.P. Kleessen B. Blaut M. Effects of inulin on faecal bifidobacteria in human subjects Br. J. Nutr. 1999 82 375 382 10.1017/S0007114599001622 10673910 · DOI
  46. [47]Smith B.J. Miller R.A. Ericsson A.C. Harrison D.C. Strong R. Schmidt T.M. Changes in the gut microbiome and fermentation products concurrent with enhanced longevity in acarbose-treated mice BMC Microbiol. 2019 19 130 10.1186/s12866-019-1494-7 31195972 PMC6567620 · DOI
  47. [48]Guilloteau P. Martin L. Eeckhaut V. Ducatelle R. Zabielski R. Van Immerseel F. From the gut to the peripheral tissues: The multiple effects of butyrate Nutr. Res. Rev. 2010 23 366 384 10.1017/S0954422410000247 20937167 · DOI
  48. [49]Salimi V. Shahsavari Z. Safizadeh B. Hosseini A. Khademian N. Tavakoli-Yaraki M. Sodium butyrate promotes apoptosis in breast cancer cells through reactive oxygen species (ROS) formation and mitochondrial impairment Lipids Health Dis. 2017 16 208 10.1186/s12944-017-0593-4 29096636 PMC5669027 · DOI
  49. [50]Zou F. Qiu Y. Huang Y. Zou H. Cheng X. Niu Q. Luo A. Sun J. Effects of short-chain fatty acids in inhibiting HDAC and activating p38 MAPK are critical for promoting B10 cell generation and function Cell Death Dis. 2021 12 582 10.1038/s41419-021-03880-9 34099635 PMC8184914 · DOI
  50. [51]Kawamura M. Goda N. Hariya N. Kimura M. Ishiyama S. Kubota T. Mochizuki K. Medium-chain fatty acids enhance expression and histone acetylation of genes related to lipid metabolism in insulin-resistant adipocytes Biochem. Biophys. Rep. 2022 29 101196 10.1016/j.bbrep.2021.101196 35028437 PMC8741418 · DOI
  51. [52]Ito K. Adcock I.M. Histone acetylation and histone deacetylation Mol. Biotechnol. 2002 20 99 106 10.1385/MB:20:1:099 11876304 · DOI
  52. [53]Fraga M.F. Ballestar E. Villar-Garea A. Boix-Chornet M. Espada J. Schotta G. Bonaldi T. Haydon C. Ropero S. Petrie K. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer Nat. Genet. 2005 37 391 400 10.1038/ng1531 15765097 · DOI
  53. [54]Lyko F. The DNA methyltransferase family: A versatile toolkit for epigenetic regulation Nat. Rev. Genet 2018 19 81 92 10.1038/nrg.2017.80 29033456 · DOI
  54. [55]Szyf M. Pakneshan P. Rabbani S.A. DNA methylation and breast cancer Biochem. Pharmacol. 2004 68 1187 1197 10.1016/j.bcp.2004.04.030 15313416 · DOI
  55. [56]Hemmings B.A. Restuccia D.F. PI3K-PKB/Akt pathway Cold Spring Harb. Perspect Biol. 2012 4 a011189 10.1101/cshperspect.a011189 22952397 PMC3428770 · DOI
  56. [57]Paplomata E. O’Regan R. The PI3K/AKT/mTOR pathway in breast cancer: Targets, trials and biomarkers Ther. Adv. Med. Oncol. 2014 6 154 166 10.1177/1758834014530023 25057302 PMC4107712 · DOI
  57. [58]Wang W. Nag S.A. Zhang R. Targeting the NFkappaB signaling pathways for breast cancer prevention and therapy Curr. Med. Chem. 2015 22 264 289 10.2174/0929867321666141106124315 25386819 PMC6690202 · DOI
  58. [59]Bessou M. Lopez J. Gadet R. Deygas M. Popgeorgiev N. Poncet D. Nougarede A. Billard P. Mikaelian I. Gonzalo P. The apoptosis inhibitor Bcl-xL controls breast cancer cell migration through mitochondria-dependent reactive oxygen species production Oncogene 2020 39 3056 3074 10.1038/s41388-020-1212-9 32066881 · DOI
  59. [60]Thu K.L. Soria-Bretones I. Mak T.W. Cescon D.W. Targeting the cell cycle in breast cancer: Towards the next phase Cell Cycle 2018 17 1871 1885 10.1080/15384101.2018.1502567 30078354 PMC6152498 · DOI
  60. [61]Filippone A. Casili G. Scuderi S.A. Mannino D. Lanza M. Campolo M. Paterniti I. Capra A.P. Colarossi C. Bonasera A. Sodium Propionate Contributes to Tumor Cell Growth Inhibition through PPAR-gamma Signaling Cancers 2022 15 217 10.3390/cancers15010217 36612214 PMC9818202 · DOI
  61. [62]Li Y. Buckhaults P. Li S. Tollefsbol T. Temporal Efficacy of a Sulforaphane-Based Broccoli Sprout Diet in Prevention of Breast Cancer through Modulation of Epigenetic Mechanisms Cancer Prev. Res. 2018 11 451 464 10.1158/1940-6207.CAPR-17-0423 PMC6072582 29764806 · DOI
  62. [63]Chen M. Li S. Srinivasasainagendra V. Sharma M. Li Z. Tiwari H. Tollefsbol T.O. Li Y. Maternal soybean genistein on prevention of later-life breast cancer through inherited epigenetic regulations Carcinogenesis 2022 43 190 202 10.1093/carcin/bgac009 35084457 PMC9036993 · DOI
  63. [64]Brane A. Arora I. Tollefsbol T.O. Peripubertal Nutritional Prevention of Cancer-Associated Gene Expression and Phenotypes Cancers 2023 15 674 10.3390/cancers15030674 36765634 PMC9913820 · DOI
  64. [65]Li S. Wu H. Tollefsbol T.O. Combined Broccoli Sprouts and Green Tea Polyphenols Contribute to the Prevention of Estrogen Receptor-Negative Mammary Cancer via Cell Cycle Arrest and Inducing Apoptosis in HER2/neu Mice J. Nutr. 2021 151 73 84 10.1093/jn/nxaa315 33188406 PMC7779229 · DOI
  65. [66]Kumar R. Eipers P. Little R.B. Crowley M. Crossman D.K. Lefkowitz E.J. Morrow C.D. Getting started with microbiome analysis: Sample acquisition to bioinformatics Curr. Protoc. Hum. Genet 2014 82 11 18 10.1002/0471142905.hg1808s82 25042718 PMC4383038 · DOI
  66. [67]Paul B. Royston K.J. Li Y. Stoll M.L. Skibola C.F. Wilson L.S. Barnes S. Morrow C.D. Tollefsbol T.O. Impact of genistein on the gut microbiome of humanized mice and its role in breast tumor inhibition PLoS ONE 2017 12 e0189756 10.1371/journal.pone.0189756 29267377 PMC5739415 · DOI
  67. [68]Caporaso J.G. Lauber C.L. Walters W.A. Berg-Lyons D. Lozupone C.A. Turnbaugh P.J. Fierer N. Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample Proc. Natl. Acad. Sci. USA 2011 108 (Suppl. S1) 4516 4522 10.1073/pnas.1000080107 20534432 PMC3063599 · DOI
  68. [69]Caporaso J.G. Bittinger K. Bushman F.D. DeSantis T.Z. Andersen G.L. Knight R. PyNAST: A flexible tool for aligning sequences to a template alignment Bioinformatics 2010 26 266 267 10.1093/bioinformatics/btp636 19914921 PMC2804299 · DOI
  69. [70]Lozupone C. Knight R. UniFrac: A new phylogenetic method for comparing microbial communities Appl. Environ. Microbiol. 2005 71 8228 8235 10.1128/AEM.71.12.8228-8235.2005 16332807 PMC1317376 · DOI · Paper page
  70. [71]Han J. Lin K. Sequeira C. Borchers C.H. An isotope-labeled chemical derivatization method for the quantitation of short-chain fatty acids in human feces by liquid chromatography-tandem mass spectrometry Anal. Chim. Acta 2015 854 86 94 10.1016/j.aca.2014.11.015 25479871 · DOI

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  • Drug repurposing for cancer therapy

    Xia, Y., Sun, M., Huang, H., & Jin, W.-L. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01808-1 · Cited by 443 · see citing works

    “225 Furthermore, inulin has been credited with fostering the proliferation of bene fi cial gut fl ora while impeding the growth of deleterious bacteria in an animal model harboring the murine pks + E. coli strain NC101.”
    Background

Authors
Wu, H., Van Der Pol, W. J., Dubois, L. G., Morrow, C. D., & Tollefsbol, T. O.
Affiliations
  • University of Alabama at Birmingham (US)
  • Center for Clinical and Translational Science, University of Alabama at Birmingham, Birmingham, AL 35233, USA
  • Duke Medical Center (US)
Corresponding author
Tollefsbol, Trygve O.
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2023-05-19
Volume
24
Issue
10
Pages
9015
ISSN
1422-0067 (ISSN-L)
DOI
10.3390/ijms24109015
PMC
PMC10218871
OpenAlex
W4377092509
Cited by
27
References
1
Citations by year
2026: 6 · 2025: 11 · 2024: 7 · 2023: 3
FWCI
4.72
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Institutes of Health (NCI R01 CA178441, NCI R01 CA204346)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords
inulin, dietary supplementation, breast cancer prevention, gut microbiota, short-chain fatty acids, propionic acid, sodium propionate, HDAC2, HDAC8, DNMT3B, epigenetic regulation, Akt signaling, NF-κB signaling, PI3K/Akt signaling, tumor growth inhibition, transgenic mouse model
MeSH terms
Gastrointestinal Microbiome, Animals, Female, Inulin, Neoplasms, Receptors, Estrogen, Dietary Supplements, Epigenesis, Genetic, Mice, Prebiotics, Microbiota

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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