2,000
Views
2
CrossRef citations to date
0
Altmetric
Research Paper

Colorectal cancer–associated T cell receptor repertoire abnormalities are linked to gut microbiome shifts and somatic cell mutations

, , , , , , , , , ORCID Icon & show all
Article: 2263934 | Received 01 Jun 2023, Accepted 24 Sep 2023, Published online: 05 Oct 2023

References

  • Wong SH, Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat Rev Gastro Hepat. 2019;16(11):690–22. doi:10.1038/s41575-019-0209-8.
  • Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K. Environmental and heritable factors in the causation of cancer — analyses of Cohorts of Twins from Sweden, Denmark, and Finland. N Engl J Med. 2000;343(2):78–85. doi:10.1056/NEJM200007133430201.
  • Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, Reading N, Villablanca E, Wang S, Mora J, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012;149(7):1578–1593. doi:10.1016/j.cell.2012.04.037.
  • Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90. doi:10.3322/caac.20107.
  • Feng Q, Liang S, Jia H, Stadlmayr A, Tang L, Lan Z, Zhang D, Xia H, Xu X, Jie Z, et al. Gut microbiome development along the colorectal adenoma–carcinoma sequence. Nat Commun. 2015;6(1):6528. doi:10.1038/ncomms7528.
  • Yang Y, Weng W, Peng J, Hong L, Yang L, Toiyama Y, Gao R, Liu M, Yin M, Pan C, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating toll-like receptor 4 signaling to nuclear Factor−κB, and up-regulating expression of MicroRNA-21. Gastroenterology. 2017;152(4):851–866.e24. doi:10.1053/j.gastro.2016.11.018.
  • Sommer F, Backhed F. The gut microbiota — masters of host development and physiology. Nat Rev Microbiol. 2013;11(4):227–238. doi:10.1038/nrmicro2974.
  • Zheng DW, Dong X, Pan P, Chen KW, Fan JX, Cheng SX, Zhang X-Z. Phage-guided modulation of the gut microbiota of mouse models of colorectal cancer augments their responses to chemotherapy. Nat Biomed Eng. 2019;3(9):717–728. doi:10.1038/s41551-019-0423-2.
  • Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host & Microbe. 2014;15(3):317–328. doi:10.1016/j.chom.2014.02.007.
  • Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients. Sci. 2018;359(6371):97–103. doi:10.1126/science.aan4236.
  • Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, Gavert N, Zwang Y, Cooper ZA, Shee K, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Sci. 2017;357(6356):1156–1160. doi:10.1126/science.aah5043.
  • Zheng DW, Chen Y, Li ZH, Xu L, Li CX, Li B, Fan J-X, Cheng S-X, Zhang X-Z. Optically-controlled bacterial metabolite for cancer therapy. Nat Commun. 2018;9(1):1680. doi:10.1038/s41467-018-03233-9.
  • Fan JX, Li ZH, Liu XH, Zheng DW, Chen Y, Zhang XZ. Bacteria-mediated tumor therapy utilizing photothermally-controlled TNF-α expression via oral administration. Nano Lett. 2018;18(4):2373–2380. doi:10.1021/acs.nanolett.7b05323.
  • Liu X, Cui Y, Zhang Y, Liu Z, Zhang Q, Wu W, Zheng Z, Li S, Zhang Z, Li Y, et al. A comprehensive study of immunology repertoires in both preoperative stage and postoperative stage in patients with colorectal cancer. Molec Gen & Gen Med. 2019;7(3):e504. doi:10.1002/mgg3.504.
  • Mercader M, Bodner BK, Moser MT, Kwon PS, Park ES, Manecke RG, Ellis TM, Wojcik EM, Yang D, Flanigan RC, et al. T cell infiltration of the prostate induced by androgen withdrawal in patients with prostate cancer. Proc Natl Acad Sci USA. 2001;98(25):14565–14570. doi:10.1073/pnas.251140998.
  • Jia Q, Zhou J, Chen G, Shi Y, Yu H, Guan P, Lin R, Jiang N, Yu P, Li Q-J, et al. Diversity index of mucosal resident T lymphocyte repertoire predicts clinical prognosis in gastric cancer. Oncoimmunology. 2015;4(4):e1001230. doi:10.1080/2162402X.2014.1001230.
  • Speranza E, Ruibal P, Port JR, Feng F, Burkhardt L, Grundhoff A, Günther S, Oestereich L, Hiscox JA, Connor JH, et al. T-Cell receptor diversity and the control of T-Cell homeostasis Mark Ebola virus disease survival in humans. J Infect Dis. 2018;218(suppl_5):S508–S18. doi:10.1093/infdis/jiy352.
  • Shao H, Ou Y, Wang T, Shen H, Wu F, Zhang W, Tao C, Yuan Y, Bo H, Wang H, et al. Differences in TCR-Vβ repertoire and effector phenotype between tumor infiltrating lymphocytes and peripheral blood lymphocytes increase with Age. PloS One. 2014;9(7):e102327. doi:10.1371/journal.pone.0102327.
  • Cremonesi E, Governa V, Garzon JFG, Mele V, Amicarella F, Muraro MG, Trella E, Galati-Fournier V, Oertli D, Däster SR, et al. Gut microbiota modulate T cell trafficking into human colorectal cancer. Gut. 2018;67(11):1984–1994. doi:10.1136/gutjnl-2016-313498.
  • Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, Thangaraju M, Prasad P, Manicassamy S, Munn D, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40(1):128–139. doi:10.1016/j.immuni.2013.12.007.
  • Cani PD, Jordan BF. Gut microbiota-mediated inflammation in obesity: a link with gastrointestinal cancer. Nat Rev Gastro Hepat. 2018;15(11):671–682. doi:10.1038/s41575-018-0025-6.
  • Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, et al. The genomic landscapes of human breast and colorectal cancers. Sci. 2007;318(5853):1108–1113. doi:10.1126/science.1145720.
  • Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, et al. The consensus coding sequences of human breast and colorectal cancers. Sci. 2006;314(5797):268–274. doi:10.1126/science.1133427.
  • Bass AJ, Lawrence MS, Brace LE, Ramos AH, Drier Y, Cibulskis K, Sougnez C, Voet D, Saksena G, Sivachenko A, et al. Genomic sequencing of colorectal adenocarcinomas identifies a recurrent VTI1A-TCF7L2 fusion. Nat Genet. 2011;43(10):964–968. doi:10.1038/ng.936.
  • Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol. 2011;6(1):479–507. doi:10.1146/annurev-pathol-011110-130235.
  • Zaidi SH, Harrison TA, Phipps AI, Steinfelder R, Trinh QM, Qu C, Banbury BL, Georgeson P, Grasso CS, Giannakis M, et al. Landscape of somatic single nucleotide variants and indels in colorectal cancer and impact on survival. Nat Commun. 2020;11(1):3644. doi:10.1038/s41467-020-17386-z.
  • Chang YS, Lee CC, Ke TW, Chang CM, Chao DS, Huang HY, Chang J-G. Molecular characterization of colorectal cancer using whole-exome sequencing in a Taiwanese population. Cancer Med. 2019;8(8):3738–3747. doi:10.1002/cam4.2282.
  • Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host & Microbe. 2013;14:195–206. doi:10.1016/j.chom.2013.07.012.
  • Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M, Inamura K, Kim SA, Masuda A, Nowak JA, Nosho K, et al. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol. 2015;1(5):653–661. doi:10.1001/jamaoncol.2015.1377.
  • Tomkovich S, Yang Y, Winglee K, Gauthier J, Muhlbauer M, Sun X, Mohamadzadeh M, Liu X, Martin P, Wang GP, et al. Locoregional effects of microbiota in a preclinical model of Colon carcinogenesis. Cancer Res. 2017;77(10):2620–2632. doi:10.1158/0008-5472.CAN-16-3472.
  • Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy T, Chung D, Lochhead P, Hold G, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host & Microbe. 2013;14(2):207–215. doi:10.1016/j.chom.2013.07.007.
  • Cui JH, Lin KR, Yuan SH, Jin YB, Chen XP, Su XK, Jiang J, Pan Y-M, Mao S-L, Mao X-F, et al. TCR repertoire as a novel indicator for immune monitoring and prognosis assessment of patients with cervical cancer. Front Immunol. 2018;9:2729. doi:10.3389/fimmu.2018.02729.
  • Chen Z, Zhang C, Pan Y, Xu R, Xu C, Chen Z, Lu Z, Ke Y. T cell receptor β-chain repertoire analysis reveals intratumour heterogeneity of tumour-infiltrating lymphocytes in oesophageal squamous cell carcinoma. J Pathol. 2016;239(4):450–458. doi:10.1002/path.4742.
  • Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi:10.1038/nature08821.
  • Bazzi ZA, Sneddon S, Zhang PGY, Tai IT. Characterization of the immune cell landscape in CRC: clinical implications of tumour-infiltrating leukocytes in early- and late-stage CRC. Front Immunol. 2022;13:978862. doi:10.3389/fimmu.2022.978862.
  • Gelsomino F, Barbolini M, Spallanzani A, Pugliese G, Cascinu S. The evolving role of microsatellite instability in colorectal cancer: a review. Cancer Treat Rev. 2016;51:19–26. doi:10.1016/j.ctrv.2016.10.005.
  • Sanz-Pamplona R, Melas M, Maoz A, Schmit SL, Rennert H, Lejbkowicz F, Greenson JK, Sanjuan X, Lopez-Zambrano M, Alonso MH, et al. Lymphocytic infiltration in stage II microsatellite stable colorectal tumors: a retrospective prognosis biomarker analysis. PLoS Med. 2020;17(9):e1003292. doi:10.1371/journal.pmed.1003292.
  • Yachida S, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, Watanabe H, Masuda K, Nishimoto Y, Kubo M, et al. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat Med. 2019;25(6):968–976. doi:10.1038/s41591-019-0458-7.
  • Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52(6):2141–2146. doi:10.1099/00207713-52-6-2141.
  • Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microb. 2004;70(10):5810–5817. doi:10.1128/AEM.70.10.5810-5817.2004.
  • Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, Boselli L, Routier E, Cassard L, Collins M, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol : Off J Eur Soc Medi Oncol. 2017;28(6):1368–1379. doi:10.1093/annonc/mdx108.
  • Frankel AE, Coughlin LA, Kim J, Froehlich TW, Xie Y, Frenkel EP, Koh AY. Metagenomic shotgun sequencing and unbiased metabolomic profiling identify specific human gut microbiota and metabolites associated with immune checkpoint therapy efficacy in melanoma patients. Neoplasia. 2017;19(10):848–855. doi:10.1016/j.neo.2017.08.004.
  • Lonardi S, Munoz-Amatriain M, Liang Q, Shu S, Wanamaker SI, Lo S, Tanskanen J, Schulman AH, Zhu T, Luo M-C, et al. The genome of cowpea (vigna unguiculata [L.] Walp.). Plant J. 2019;98(5):767–782. doi:10.1111/tpj.14349.
  • Sabanadzovic S, Valverde RA, Brown JK, Martin RR, Tzanetakis IE. Southern tomato virus: the link between the families totiviridae and partitiviridae. Virus Res. 2009;140(1–2):130–137. doi:10.1016/j.virusres.2008.11.018.
  • Li RH, Zettler FW, Purcifull DE, Hiebert E. The nucleotide sequence of the 3′-terminal region of dasheen mosaic virus (Caladium isolate) and expression of its coat protein in Escherichia coli for antiserum production. Arch Virol. 1998;143(12):2461–2469. doi:10.1007/s007050050476.
  • Babu B, Hegde V. Molecular characterization of Dasheen mosaic virus isolates infecting edible aroids in India. Acta Virol. 2014;58(1):34–42. doi:10.4149/av_2014_01_34.
  • Hao Y, Samuels Y, Li Q, Krokowski D, Guan BJ, Wang C, Jin Z, Dong B, Cao B, Feng X, et al. Oncogenic PIK3CA mutations reprogram glutamine metabolism in colorectal cancer. Nat Commun. 2016;7(1):11971. doi:10.1038/ncomms11971.
  • Cao Y, Lin SH, Wang Y, Chin YE, Kang L, Mi J. Glutamic pyruvate transaminase GPT2 promotes tumorigenesis of breast cancer cells by activating sonic hedgehog signaling. Theranostics. 2017;7(12):3021–3033. doi:10.7150/thno.18992.
  • Willard SS, Koochekpour S. Glutamate signaling in benign and malignant disorders: current status, future perspectives, and therapeutic implications. Int J Biol Sci. 2013;9(7):728–742. doi:10.7150/ijbs.6475.
  • Shroff EH, Eberlin LS, Dang VM, Gouw AM, Gabay M, Adam SJ, Bellovin, DI, Tran, PT, Philbrick, WM, Garcia-Ocana, A, et al. MYC oncogene overexpression drives renal cell carcinoma in a mouse model through glutamine metabolism. Proc Natl Acad Sci U S A. 2015;112(21):6539–6544.
  • Seidlitz EP, Sharma MK, Saikali Z, Ghert M, Singh G. Cancer cell lines release glutamate into the extracellular environment. Clin Exp Metastasis. 2009;26(7):781–787. doi:10.1007/s10585-009-9277-4.
  • Collins CL, Wasa M, Souba WW, Abcouwer SF. Determinants of glutamine dependence and utilization by normal and tumor-derived breast cell lines. J Cell Physiol. 1998;176(1):166–178. doi:10.1002/(SICI)1097-4652(199807)176:1<166:AID-JCP18>3.0.CO;2-5.
  • Karlsson FH, Tremaroli V, Nookaew I, Bergstrom G, Behre CJ, Fagerberg B, Nielsen J, Bäckhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498(7452):99–103. doi:10.1038/nature12198.
  • Ito M, Kanno S, Nosho K, Sukawa Y, Mitsuhashi K, Kurihara H, Igarashi H, Takahashi T, Tachibana M, Takahashi H, et al. Association of Fusobacterium nucleatum with clinical and molecular features in colorectal serrated pathway. Int J Cancer. 2015;137(6):1258–1268. doi:10.1002/ijc.29488.
  • Zhang S, Yang Y, Weng W, Guo B, Cai G, Ma Y, Cai S. Fusobacterium nucleatum promotes chemoresistance to 5-fluorouracil by upregulation of BIRC3 expression in colorectal cancer. J Exp Clin Cancer Res. 2019;38(1):14. doi:10.1186/s13046-018-0985-y.
  • Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, Enk J, Bar-On Y, Stanietsky-Kaynan N, Coppenhagen-Glazer S, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 2015;42(2):344–355. doi:10.1016/j.immuni.2015.01.010.
  • Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60. doi:10.1038/nature11450.
  • Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSpades: a new versatile metagenomic assembler. Genome Res. 2017;27(5):824–834. doi:10.1101/gr.213959.116.
  • Zhu W, Lomsadze A, Borodovsky M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 2010;38(12):e132. doi:10.1093/nar/gkq275.
  • Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60. doi:10.1038/nmeth.3176.
  • 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.
  • Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto J-M, Kennedy S, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–546. doi:10.1038/nature12506.
  • Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J, Sunagawa S, Plichta DR, Gautier L, Pedersen AG, Le Chatelier E, et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol. 2014;32(8):822–828. doi:10.1038/nbt.2939.