695
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Prevotella copri exhausts intrinsic indole-3-pyruvic acid in the host to promote breast cancer progression: inactivation of AMPK via UHRF1-mediated negative regulation

, , , , , , , , , , , , & show all
Article: 2347757 | Received 08 Jul 2023, Accepted 22 Apr 2024, Published online: 21 May 2024

References

  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA A Cancer J Clinicians. 2021;71(3):209–27. doi:10.3322/caac.21660.
  • Derakhshan F, Reis-Filho JS. Pathogenesis of triple-negative breast cancer. Annu Rev Pathol. 2022;17(1):181–204. doi:10.1146/annurev-pathol-042420-093238.
  • Houghton SC, Hankinson SE. Cancer progress and priorities: breast cancer. Cancer Epidemiol Biomarkers Prev. 2021;30(5):822–844. doi:10.1158/1055-9965.EPI-20-1193.
  • Loibl S, Poortmans P, Morrow M, Denkert C, Curigliano G. Breast cancer. Lancet. 2021;397(10286):1750–1769. doi:10.1016/S0140-6736(20)32381-3.
  • Lau HCH, Sung JJ, Yu J. Gut microbiota: impacts on gastrointestinal cancer immunotherapy. Gut Microbes. 2021;13(1):1–21. doi:10.1080/19490976.2020.1869504.
  • Schwabe RF, Greten TF. Gut microbiome in HCC – mechanisms, diagnosis and therapy. J Hepatol. 2020;72(2):230–238. doi:10.1016/j.jhep.2019.08.016.
  • Pan LL, Li BB, Pan XH, Sun J. Gut microbiota in pancreatic diseases: possible new therapeutic strategies. Acta Pharmacol Sin. 2020;42(7):1027–1039. doi:10.1038/s41401-020-00532-0.
  • Zhu J, Liao M, Yao Z, Liang W, Li Q, Liu J, Yang H, Ji Y, Wei W, Tan A. et al. Breast cancer in postmenopausal women is associated with an altered gut metagenome. Microbiome. 2018;6(1):136. doi:10.1186/s40168-018-0515-3.
  • Yu Q, Newsome RC, Beveridge M, Hernandez MC, Gharaibeh RZ, Jobin C, Thomas RM. Intestinal microbiota modulates pancreatic carcinogenesis through intratumoral natural killer cells. Gut Microbes. 2022;14(1):2112881. doi:10.1080/19490976.2022.2112881.
  • Baruch EN, Youngster I, Ben-Betzalel G, Ortenberg R, Lahat A, Katz L, Adler K, Dick-Necula D, Raskin S, Bloch N. et al. Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science. 2020;6529(2021):602–609.
  • Daillère R, Vétizou M, Waldschmitt N, Yamazaki T, Isnard C, Poirier-Colame V, Duong CM, Flament C, Lepage P, Roberti M. et al. Enterococcus hirae and Barnesiella intestinihominis Facilitate Cyclophosphamide-Induced Therapeutic Immunomodulatory Effects. Immunity. 2016;45(4):931–943. doi:10.1016/j.immuni.2016.09.009.
  • Guo H, Chou WC, Lai Y, Liang K, Tam JW, Brickey WJ, Chen L, Montgomery ND, Li X, Bohannon LM. et al. Multi-omics analyses of radiation survivors identify radioprotective microbes and metabolites. Science. 2020;370(6516):370. doi:10.1126/science.aay9097.
  • Di Modica M, Gargari G, Regondi V, Bonizzi A, Arioli S, Belmonte B, De Cecco L, Fasano E, Bianchi F, Bertolotti A. et al. Gut microbiota condition the therapeutic efficacy of trastuzumab in HER2-positive breast cancer. Cancer Res. 2021;81(8):2195–2206. doi:10.1158/0008-5472.CAN-20-1659.
  • Urbaniak C, Gloor GB, Brackstone M, Scott L, Tangney M, Reid G, Goodrich-Blair H. The microbiota of Breast Tissue and its association with Breast cancer. Appl Environ Microb. 2016;82(16):5039–5048. doi:10.1128/AEM.01235-16.
  • Fu A, Yao B, Dong T, Chen Y, Yao J, Liu Y, Li H, Bai H, Liu X, Zhang Y. et al. Tumor-resident intracellular microbiota promotes metastatic colonization in breast cancer. Cell. 2022;185(8):1356–1372.e26. doi:10.1016/j.cell.2022.02.027.
  • Ma J, Sun L, Liu Y, Ren H, Shen Y, Bi F, Zhang T, Wang X. Alter between gut bacteria and blood metabolites and the anti-tumor effects of faecalibacterium prausnitzii in breast cancer. BMC Microbiol. 2020;20(1):82. doi:10.1186/s12866-020-01739-1.
  • Wang H, Rong X, Zhao G, Zhou Y, Xiao Y, Ma D, Jin X, Wu Y, Yan Y, Yang H. et al. The microbial metabolite trimethylamine N-oxide promotes antitumor immunity in triple-negative breast cancer. Cell Metab. 2022;34(4):581–594.e8. doi:10.1016/j.cmet.2022.02.010.
  • De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA. 2010;107(33):14691–14696. doi:10.1073/pnas.1005963107.
  • Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP. et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227. doi:10.1038/nature11053.
  • Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto J-M. et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180. doi:10.1038/nature09944.
  • O’Connor JB, Mottlowitz M, Kruk ME, Mickelson A, Wagner BD, Harris JK, Wendt CH, Laguna TA. Network analysis to identify multi-omic correlations in the Lower Airways of children with cystic fibrosis. Front Cell Infect Microbiol. 2022;12:805170. doi:10.3389/fcimb.2022.805170.
  • Eriksson K, Lundmark A, Delgado LF, Hu YOO, Fei G, Lee L, Fei C, Catrina AI, Jansson L, Andersson AF. et al. Salivary microbiota and host-inflammatory responses in periodontitis affected individuals with and without rheumatoid arthritis. Front Cell Infect Microbiol. 2022;12:841139. doi:10.3389/fcimb.2022.841139.
  • Chu Y, Sun S, Huang Y, Gao Q, Xie X, Wang P, Li J, Liang L, He X, Jiang Y. et al. Metagenomic analysis revealed the potential role of gut microbiome in gout. npj Biofilms Microbiomes. 2021;7(1):66–. doi:10.1038/s41522-021-00235-2.
  • Dong TS, Guan M, Mayer EA, Stains J, Liu C, Vora P, Jacobs JP, Lagishetty V, Chang L, Barry RL. et al. Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center. Gut Microbes. 2022;14(1):2051999. doi:10.1080/19490976.2022.2051999.
  • Jiang L, Shang M, Yu S, Liu Y, Zhang H, Zhou Y, Wang M, Wang T, Li H, Liu Z. et al. A high-fiber diet synergizes with Prevotella copri and exacerbates rheumatoid arthritis. Cell Mol Immunol. 2022;19(12):1414–1424. doi:10.1038/s41423-022-00934-6.
  • Tett A, Pasolli E, Masetti G, Ercolini D, Segata N. Prevotella diversity, niches and interactions with the human host. Nat Rev Microbiol. 2021;19(9):585–599. doi:10.1038/s41579-021-00559-y.
  • Tett A, Huang KD, Asnicar F, Fehlner-Peach H, Pasolli E, Karcher N, Armanini F, Manghi P, Bonham K, Zolfo M. et al. The prevotella copri complex comprises four distinct clades underrepresented in westernized populations. Cell Host Microbe. 2019;26(5):666–79.e7. doi:10.1016/j.chom.2019.08.018.
  • Mao AW, Barck H, Young J, Paley A, Mao J, Chang H. Identification of a novel cancer microbiome signature for predicting prognosis of human breast cancer patients. Clin Transl Oncol. 2021;24(3):597–604. doi:10.1007/s12094-021-02725-3.
  • Pasolli E, Asnicar F, Manara S, Zolfo M, Karcher N, Armanini F, Beghini F, Manghi P, Tett A, Ghensi P. et al. Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell. 2019;176(3):649–62.e20. doi:10.1016/j.cell.2019.01.001.
  • Su J, Su L, Li D, Shuai O, Zhang Y, Liang H, Jiao C, Xu Z, Lai Y, Xie Y. et al. Antitumor activity of extract from the sporoderm-breaking spore of ganoderma lucidum: restoration on exhausted cytotoxic T cell with gut microbiota remodeling. Front Immunol. 2018;9:1765. doi:10.3389/fimmu.2018.01765.
  • Su J, Li D, Chen Q, Li M, Su L, Luo T, Liang D, Lai G, Shuai O, Jiao C. et al. Anti-breast cancer enhancement of a polysaccharide from spore of ganoderma lucidum with paclitaxel: suppression on tumor metabolism with gut microbiota reshaping. Front Microbiol. 2018;9:3099. doi:10.3389/fmicb.2018.03099.
  • Sidhu H, Capalash N. UHRF1: the key regulator of epigenetics and molecular target for cancer therapeutics. Tumour Biol. 2017;39(2):1010428317692205. doi:10.1177/1010428317692205.
  • Inoki K, Kim J, Guan KL. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu Rev Pharmacol Toxicol. 2012;52(1):381–400. doi:10.1146/annurev-pharmtox-010611-134537.
  • Hu CA, Wu Z, Wang J. Amino acids and autophagy: their crosstalk, interplay and interlock. Amino Acids. 2015;47(10):2035–2036. doi:10.1007/s00726-015-2098-7.
  • Tintelnot J, Xu Y, Lesker TR, Schonlein M, Konczalla L, Giannou AD, Pelczar P, Kylies D, Puelles VG, Bielecka AA. et al. Microbiota-derived 3-IAA influences chemotherapy efficacy in pancreatic cancer. Nature. 2023;615(7950):168–174. doi:10.1038/s41586-023-05728-y.
  • Xu X, Ding G, Liu C, Ding Y, Chen X, Huang X, Zhang C-S, Lu S, Zhang Y, Huang Y. et al. Nuclear UHRF1 is a gate-keeper of cellular AMPK activity and function. Cell Res. 2022;32(1):54–71. doi:10.1038/s41422-021-00565-y.
  • Shah HN, Collins DM. Prevotella, a new genus to include bacteroides melaninogenicus and related species formerly classified in the genus bacteroides. Int J Syst Bacteriol. 1990;40(2):205–208. doi:10.1099/00207713-40-2-205.
  • Oliver WW, Wherry WB. Notes on some bacterial parasites of the human mucous membranes. J Infect Dis. 1921;34(4):341–344. doi:10.1093/infdis/28.4.341.
  • Alpizar-Rodriguez D, Lesker TR, Gronow A, Gilbert B, Raemy E, Lamacchia C, Gabay C, Finckh A, Strowig T. Prevotella copri in individuals at risk for rheumatoid arthritis. Ann Rheum Dis. 2019;78(5):590–593. doi:10.1136/annrheumdis-2018-214514.
  • Pianta A, Arvikar S, Strle K, Drouin EE, Wang Q, Costello CE, Steere AC. Evidence of the immune relevance of Prevotella copri, a gut microbe, in patients with rheumatoid arthritis. Arthritis & Rheumatol (Hoboken, NJ). 2017;69(5):964–975. doi:10.1002/art.40003.
  • Wen C, Zheng Z, Shao T, Liu L, Xie Z, Le Chatelier E, He Z, Zhong W, Fan Y, Zhang L. et al. Quantitative metagenomics reveals unique gut microbiome biomarkers in ankylosing spondylitis. Genome Biol. 2017;18(1):142. doi:10.1186/s13059-017-1271-6.
  • Chandrashekar DS, Bashel B, Balasubramanya SAH, Creighton CJ, Ponce-Rodriguez I, Chakravarthi B, Varambally S. UALCAN: a portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia (New York, NY). 2017;19(8):649–658. doi:10.1016/j.neo.2017.05.002.
  • Gao SP, Sun HF, Li LD, Fu WY, Jin W. UHRF1 promotes breast cancer progression by suppressing KLF17 expression by hypermethylating its promoter. Am J Cancer Res. 2017;7:1554–1565.
  • Chen H, Ma H, Inuzuka H, Diao J, Lan F, Shi YG, Wei W, Shi Y. DNA damage regulates UHRF1 stability via the SCF β-TrCP E3 ligase. Mol Cell biol. 2013;33(6):1139–1148. doi:10.1128/MCB.01191-12.
  • Vaughan RM, Dickson BM, Whelihan MF, Johnstone AL, Cornett EM, Cheek MA, Ausherman CA, Cowles MW, Sun Z-W, Rothbart SB. Chromatin structure and its chemical modifications regulate the ubiquitin ligase substrate selectivity of UHRF1. Proc Natl Acad Sci USA. 2018;115(35):8775–8780. doi:10.1073/pnas.1806373115.
  • Karlsson M, Zhang C, Méar L, Zhong W, Digre A, Katona B, Sjöstedt E, Butler L, Odeberg J, Dusart P. et al. A single–cell type transcriptomics map of human tissues. Sci Adv. 2021;7(31):eabh2169. doi:10.1126/sciadv.abh2169.
  • Meilinger D, Fellinger K, Bultmann S, Rothbauer U, Bonapace IM, Klinkert WE, Spada F, Leonhardt H. Np95 interacts with de novo DNA methyltransferases, Dnmt3a and Dnmt3b, and mediates epigenetic silencing of the viral CMV promoter in embryonic stem cells. EMBO Rep. 2009;10(11):1259–1264. doi:10.1038/embor.2009.201.
  • Bostick M, Kim JK, Estève PO, Clark A, Pradhan S, Jacobsen SE. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science. 2007;317(5845):1760–1764. doi:10.1126/science.1147939.
  • Nishiyama A, Nakanishi M. Navigating the DNA methylation landscape of cancer. Trends Genet. 2021;37(11):1012–1027. doi:10.1016/j.tig.2021.05.002.
  • Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet. 2007;8(4):286–298. doi:10.1038/nrg2005.
  • Agus A, Planchais J, Sokol H. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe. 2018;23(6):716–724. doi:10.1016/j.chom.2018.05.003.
  • Rao Z, Li J, Shi B, Zeng Y, Liu Y, Sun Z, Wu L, Sun W, Tang Z. Dietary tryptophan levels impact growth performance and intestinal microbial ecology in weaned piglets via tryptophan metabolites and intestinal antimicrobial peptides. Anim: An Open Access J MDPI. 2021;11(3):11. doi:10.3390/ani11030817.
  • Liang H, Dai Z, Liu N, Ji Y, Chen J, Zhang Y, Yang Y, Li J, Wu Z, Wu G. et al. Dietary L-Tryptophan modulates the structural and functional composition of the intestinal microbiome in weaned piglets. Front Microbiol. 2018;9:1736. doi:10.3389/fmicb.2018.01736.
  • Bender MJ, McPherson AC, Phelps CM, Pandey SP, Laughlin CR, Shapira JH, Medina Sanchez L, Rana M, Richie TG, Mims TS. et al. Dietary tryptophan metabolite released by intratumoral lactobacillus reuteri facilitates immune checkpoint inhibitor treatment. Cell. 2023;186(9):1846–1862.e26. doi:10.1016/j.cell.2023.03.011.
  • Yuan J, Dong X, Yap J, Hu J. The MAPK and AMPK signalings: interplay and implication in targeted cancer therapy. J Hematol Oncol. 2020;13(1):113. doi:10.1186/s13045-020-00949-4.
  • El-Houjeiri L, Biondini M, Paquette M, Kuasne H, Pacis A, Park M, Siegel PM, Pause A. Folliculin impairs breast tumor growth by repressing TFE3-dependent induction of the Warburg effect and angiogenesis. J Clin Invest. 2021;131(22):131. doi:10.1172/JCI144871.
  • Chen LM, Yang PP, Al Haq AT, Hwang PA, Lai YC, Weng YS, Chen MA, Hsu H-L. Oligo-Fucoidan supplementation enhances the effect of olaparib on preventing metastasis and recurrence of triple-negative breast cancer in mice. J Biomed Sci. 2022;29(1):70. doi:10.1186/s12929-022-00855-6.
  • Hezaveh K, Shinde RS, Klotgen A, Halaby MJ, Lamorte S, Ciudad MT, Quevedo R, Neufeld L, Liu ZQ, Jin R. et al. Tryptophan-derived microbial metabolites activate the aryl hydrocarbon receptor in tumor-associated macrophages to suppress anti-tumor immunity. Immunity. 2022;55(2):324–340.e8. doi:10.1016/j.immuni.2022.01.006.
  • Iizuka T, Yin P, Zuberi A, Kujawa S, Coon J, Bjorvang RD, Damdimopoulou P, Pacyga DC, Strakovsky RS, Flaws JA. et al. Mono-(2-ethyl-5-hydroxyhexyl) phthalate promotes uterine leiomyoma cell survival through tryptophan-kynurenine-AHR pathway activation. Proc Natl Acad Sci USA. 2022;119(47):e2208886119. doi:10.1073/pnas.2208886119.
  • Aoki R, Aoki-Yoshida A, Suzuki C, Takayama Y. Indole-3-Pyruvic Acid, an Aryl Hydrocarbon Receptor Activator, Suppresses Experimental Colitis in Mice. J Immunol. 2018;201(12):3683–3693. doi:10.4049/jimmunol.1701734.
  • Chen W, Wen L, Bao Y, Tang Z, Zhao J, Zhang X, Wei T, Zhang J, Ma T, Zhang Q. et al. Gut flora disequilibrium promotes the initiation of liver cancer by modulating tryptophan metabolism and up-regulating SREBP2. Proc Natl Acad Sci USA. 2022;119(52):e2203894119. doi:10.1073/pnas.2203894119.
  • Renga G, Nunzi E, Pariano M, Puccetti M, Bellet MM, Pieraccini G, D’Onofrio F, Santarelli I, Stincardini C, Aversa F. et al. Optimizing therapeutic outcomes of immune checkpoint blockade by a microbial tryptophan metabolite. J Immunother Cancer. 2022;10(3):10. doi:10.1136/jitc-2021-003725.
  • Meng Q, Qi M, Chen DZ, Yuan R, Goldberg ID, Rosen EM, Auborn K, Fan S. Suppression of breast cancer invasion and migration by indole-3-carbinol: associated with up-regulation of BRCA1 and E-cadherin/catenin complexes. J Mol Med (Berl). 2000;78(3):155–165. doi:10.1007/s001090000088.
  • Okino ST, Pookot D, Basak S, Dahiya R. Toxic and chemopreventive ligands preferentially activate distinct aryl hydrocarbon receptor pathways: implications for cancer prevention. Cancer Prev Res (Philadelphia, Pa). 2009;2(3):251–256. doi:10.1158/1940-6207.CAPR-08-0146.
  • Wattenberg LW, Loub WD. Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res. 1978;38:1410–1413.
  • Donovan MG, Selmin OI, Romagnolo DF. Aryl hydrocarbon receptor diet and breast cancer risk. Yale J Biol Med. 2018;91:105–127.
  • Guan X, Ma F, Sun X, Li C, Li L, Liang F, Li S, Yi Z, Liu B, Xu B. et al. Gut microbiota profiling in patients with HER2-negative metastatic breast cancer receiving metronomic chemotherapy of capecitabine compared to those under conventional dosage. Front Oncol. 2020;10:10. doi:10.3389/fonc.2020.00902.
  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi:10.1038/s41587-019-0209-9.
  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M, Bates ST, Bruns TD, Bengtsson‐Palme J, Callaghan TM. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22(21):5271–5277. doi:10.1111/mec.12481.
  • Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–3066. doi:10.1093/nar/gkf436.
  • Li Q, Yuan Q, Jiang N, Zhang Y, Su Z, Lv L, Sang X, Chen R, Feng Y, Chen Q. Dihydroartemisinin regulates immune cell heterogeneity by triggering a cascade reaction of CDK and MAPK phosphorylation. Sig Transduct Target Ther. 2022;7(1):222. doi:10.1038/s41392-022-01028-5.
  • Gao F, Zhang J, Jiang P, Gong D, Wang JW, Xia Y, Østergaard MV, Wang J, Sangild PT. Marked methylation changes in intestinal genes during the perinatal period of preterm neonates. BMC Genomics. 2014;15(1):716. doi:10.1186/1471-2164-15-716.
  • Zheng X, Chen T, Zhao A, Ning Z, Kuang J, Wang S, You Y, Bao Y, Ma X, Yu H. et al. Hyocholic acid species as novel biomarkers for metabolic disorders. Nat Commun. 2021;12(1):1487. doi:10.1038/s41467-021-21744-w.