Tumor Microbiome Diversity and Composition Influence Pancreatic Cancer Outcomes

Cell

Volumn 178, Issue 4, 2019, Pages 795-806.e12

  Riquelme, E ^a,b   Zhang, Yu ^a   Zhang, Liangliang ^a   Montiel, M ^a   Zoltan, Michelle ^a   Dong, W ^a   Quesada, Pompeyo ^a   Sahin, I ^c   Chandra, V ^a   San Lucas, Anthony ^a   Scheet, Paul ^a   Xu, Hanwen ^a   Hanash, Samir M ^a   Feng, Lei ^a   Burks, Jared K ^a   Do, Kim Anh ^a   Peterson, Christine B ^a   Nejman, Deborah ^d   Tzeng, Ching Wei D ^a   Kim, Michael P ^a   Sears, Cynthia L ^e   Ajami, N ^f   Petrosino, Joseph ^f   Wood, Laura D ^e   Maitra, Anirban ^a   Straussman, R ^d   Katz, Matthew ^a   White, James Robert ^g   Jenq, Robert ^a   Wargo, Jennifer ^a   McAllister, Florencia ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSIDAD MAYOR   (Chile)

^c TEXAS SOUTHERN UNIVERSITY   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

^g Resphera Biosciences   (United States)

Author keywords

antibiotics; cancer survivors; CD8; fecal microbial transplants; immunoactivation; microbiota; pancreatic cancer; PDAC; tumor microbiome

Indexed keywords

RNA 16S;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACILLUS CLAUSII; BACTERIUM; CLINICAL ARTICLE; COMMUNITY STRUCTURE; CONTROLLED STUDY; FECAL MICROBIOTA TRANSPLANTATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; LONG TERM SURVIVAL; MALE; MICROBIOME; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PSEUDOXANTHOMONAS; RNA SEQUENCE; SACCHAROPOLYSPORA; SHORT TERM SURVIVAL; SPECIES COMPOSITION; SPECIES DIVERSITY; STREPTOMYCES; T LYMPHOCYTE ACTIVATION; TUMOR GROWTH; TUMOR IMMUNITY; ANIMAL; C57BL MOUSE; CLASSIFICATION; COHORT ANALYSIS; FECES; GENETICS; INTESTINE FLORA; MICROBIOLOGY; MIDDLE AGED; MORTALITY; PANCREAS CARCINOMA; PANCREAS TUMOR; SEQUENCE ANALYSIS; SURVIVAL RATE; TUMOR CELL LINE;

ADULT; AGED; ANIMALS; BACTERIA; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; COHORT STUDIES; FECAL MICROBIOTA TRANSPLANTATION; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; PANCREATIC NEOPLASMS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, RNA; SURVIVAL RATE;

EID: 85069951512     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2019.07.008     Document Type: Article

References (57)

1. Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol., 11, 2010, R106.
2. Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., Fukuda, S., Saito, T., Narushima, S., Hase, K., et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500 (2013), 232–236.
3. Balachandran, V.P., Łuksza, M., Zhao, J.N., Makarov, V., Moral, J.A., Remark, R., Herbst, B., Askan, G., Bhanot, U., Senbabaoglu, Y., et al. Australian Pancreatic Cancer Genome Initiative; Garvan Institute of Medical Research; Prince of Wales Hospital; Royal North Shore Hospital;, University of Glasgow; St Vincent's Hospital; QIMR Berghofer Medical Research Institute; University of Melbourne, Centre for Cancer Research; University of Queensland, Institute for Molecular Bioscience; Bankstown Hospital; Liverpool Hospital; Royal Prince Alfred Hospital, Chris O'Brien Lifehouse; Westmead Hospital; Fremantle Hospital; St John of God Healthcare; Royal Adelaide Hospital; Flinders Medical Centre; Envoi Pathology; Princess Alexandria Hospital; Austin Hospital; Johns Hopkins Medical Institutes; ARC-Net Centre for Applied Research on Cancer. Identification of unique neoantigen qualities in long-term survivors of pancreatic cancer. Nature 551 (2017), 512–516.
4. Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., Golani, I., Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125 (2001), 279–284.
5. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
6. Cani, P.D., Gut cell metabolism shapes the microbiome. Science 357 (2017), 548–549.
7. 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 26 (2010), 266–267.
8. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
9. Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S.M., Betley, J., Fraser, L., Bauer, M., et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6 (2012), 1621–1624.
10. Dal Molin, M., Zhang, M., de Wilde, R.F., Ottenhof, N.A., Rezaee, N., Wolfgang, C.L., Blackford, A., Vogelstein, B., Kinzler, K.W., Papadopoulos, N., et al. Very Long-term Survival Following Resection for Pancreatic Cancer Is Not Explained by Commonly Mutated Genes: Results of Whole-Exome Sequencing Analysis. Clin. Cancer Res. 21 (2015), 1944–1950.
11. Daquigan, N., Seekatz, A.M., Greathouse, K.L., Young, V.B., White, J.R., High-resolution profiling of the gut microbiome reveals the extent of Clostridium difficile burden. NPJ Biofilms Microbiomes, 3, 2017, 35.
12. DeSantis, C.E., Lin, C.C., Mariotto, A.B., Siegel, R.L., Stein, K.D., Kramer, J.L., Alteri, R., Robbins, A.S., Jemal, A., Cancer treatment and survivorship statistics, 2014. CA Cancer J. Clin. 64 (2014), 252–271.
13. Devaraj, S., Hemarajata, P., Versalovic, J., The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin. Chem. 59 (2013), 617–628.
14. Drewes, J.L., White, J.R., Dejea, C.M., Fathi, P., Iyadorai, T., Vadivelu, J., Roslani, A.C., Wick, E.C., Mongodin, E.F., Loke, M.F., et al. High-resolution bacterial 16S rRNA gene profile meta-analysis and biofilm status reveal common colorectal cancer consortia. NPJ Biofilms Microbiomes, 3, 2017, 34.
15. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
16. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (2011), 2194–2200.
17. Ferretti, P., Farina, S., Cristofolini, M., Girolomoni, G., Tett, A., Segata, N., Experimental metagenomics and ribosomal profiling of the human skin microbiome. Exp. Dermatol. 26 (2017), 211–219.
18. Garrido-Laguna, I., Hidalgo, M., Pancreatic cancer: from state-of-the-art treatments to promising novel therapies. Nat. Rev. Clin. Oncol. 12 (2015), 319–334.
19. Geller, L.T., Barzily-Rokni, M., Danino, T., Jonas, O.H., Shental, N., Nejman, D., Gavert, N., Zwang, Y., Cooper, Z.A., Shee, K., et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science 357 (2017), 1156–1160.
20. Gopalakrishnan, V., Spencer, C.N., Nezi, L., Reuben, A., Andrews, M.C., Karpinets, T.V., Prieto, P.A., Vicente, D., Hoffman, K., Wei, S.C., et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359 (2018), 97–103.
21. Heller, G., The Cox proportional hazards model with a partly linear relative risk function. Lifetime Data Anal. 7 (2001), 255–277.
22. Hidalgo, M., Pancreatic cancer. N. Engl. J. Med. 362 (2010), 1605–1617.
23. Human Microbiome Project Consortium. A framework for human microbiome research. Nature 486 (2012), 215–221.
24. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
25. Kamisawa, T., Wood, L.D., Itoi, T., Takaori, K., Pancreatic cancer. Lancet 388 (2016), 73–85.
26. Kanehisa, M., Goto, S., KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28 (2000), 27–30.
27. Kim, Y.I., Park, J.E., Brand, D.D., Fitzpatrick, E.A., Yi, A.K., Protein kinase D1 is essential for the proinflammatory response induced by hypersensitivity pneumonitis-causing thermophilic actinomycetes Saccharopolyspora rectivirgula. J. Immunol. 184 (2010), 3145–3156.
28. Kuczynski, J., Stombaugh, J., Walters, W.A., Gonzalez, A., Caporaso, J.G., Knight, R., Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr. Protoc. Bioinformatics, Chapter 10, 2011, Unit 10.17.
29. Kundu, P., Blacher, E., Elinav, E., Pettersson, S., Our Gut Microbiome: The Evolving Inner Self. Cell 171 (2017), 1481–1493.
30. Kurilshikov, A., Wijmenga, C., Fu, J., Zhernakova, A., Host Genetics and Gut Microbiome: Challenges and Perspectives. Trends Immunol. 38 (2017), 633–647.
31. Langille, M.G., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Vega Thurber, R.L., Knight, R., et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31 (2013), 814–821.
32. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
33. Le, D.T., Uram, J.N., Wang, H., Bartlett, B.R., Kemberling, H., Eyring, A.D., Skora, A.D., Luber, B.S., Azad, N.S., Laheru, D., et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency. N. Engl. J. Med. 372 (2015), 2509–2520.
34. Lloyd-Price, J., Mahurkar, A., Rahnavard, G., Crabtree, J., Orvis, J., Hall, A.B., Brady, A., Creasy, H.H., McCracken, C., Giglio, M.G., et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature 550 (2017), 61–66.
35. Lozupone, C., Lladser, M.E., Knights, D., Stombaugh, J., Knight, R., UniFrac: an effective distance metric for microbial community comparison. ISME J. 5 (2011), 169–172.
36. Magoč, T., Salzberg, S.L., FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 (2011), 2957–2963.
37. Makohon-Moore, A.P., Zhang, M., Reiter, J.G., Bozic, I., Allen, B., Kundu, D., Chatterjee, K., Wong, F., Jiao, Y., Kohutek, Z.A., et al. Limited heterogeneity of known driver gene mutations among the metastases of individual patients with pancreatic cancer. Nat. Genet. 49 (2017), 358–366.
38. Manji, G.A., Olive, K.P., Saenger, Y.M., Oberstein, P., Current and Emerging Therapies in Metastatic Pancreatic Cancer. Clin. Cancer Res. 23 (2017), 1670–1678.
39. Matson, V., Fessler, J., Bao, R., Chongsuwat, T., Zha, Y., Alegre, M.L., Luke, J.J., Gajewski, T.F., The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359 (2018), 104–108.
40. Mazmanian, S.K., Round, J.L., Kasper, D.L., A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453 (2008), 620–625.
41. McAllister, F., Housseau, F., Sears, C.L., Microbiota and immune responses in colon cancer: more to learn. Cancer J. 20 (2014), 232–236.
42. McMurdie, P.J., Holmes, S., phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8, 2013, e61217.
43. Miller, K.D., Siegel, R.L., Lin, C.C., Mariotto, A.B., Kramer, J.L., Rowland, J.H., Stein, K.D., Alteri, R., Jemal, A., Cancer treatment and survivorship statistics, 2016. CA Cancer J. Clin. 66 (2016), 271–289.
44. Nieuwdorp, M., Gilijamse, P.W., Pai, N., Kaplan, L.M., Role of the microbiome in energy regulation and metabolism. Gastroenterology 146 (2014), 1525–1533.
45. Ock, C.Y., Hwang, J.E., Keam, B., Kim, S.B., Shim, J.J., Jang, H.J., Park, S., Sohn, B.H., Cha, M., Ajani, J.A., et al. Genomic landscape associated with potential response to anti-CTLA-4 treatment in cancers. Nat. Commun., 8, 2017, 1050.
46. Pushalkar, S., Hundeyin, M., Daley, D., Zambirinis, C.P., Kurz, E., Mishra, A., Mohan, N., Aykut, B., Usyk, M., Torres, L.E., et al. The Pancreatic Cancer Microbiome Promotes Oncogenesis by Induction of Innate and Adaptive Immune Suppression. Cancer Discov. 8 (2018), 403–416.
47. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 (2013), D590–D596.
48. Riquelme, E., Maitra, A., McAllister, F., Immunotherapy for Pancreatic Cancer: More Than Just a Gut Feeling. Cancer Discov. 8 (2018), 386–388.
49. Routy, B., Le Chatelier, E., Derosa, L., Duong, C.P.M., Alou, M.T., Daillère, R., Fluckiger, A., Messaoudene, M., Rauber, C., Roberti, M.P., et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359 (2018), 91–97.
50. Salzman, N.H., Hung, K., Haribhai, D., Chu, H., Karlsson-Sjöberg, J., Amir, E., Teggatz, P., Barman, M., Hayward, M., Eastwood, D., et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11 (2010), 76–83.
51. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S., Huttenhower, C., Metagenomic biomarker discovery and explanation. Genome Biol., 12, 2011, R60.
52. Shoemark, D.K., Allen, S.J., The microbiome and disease: reviewing the links between the oral microbiome, aging, and Alzheimer's disease. J. Alzheimers Dis. 43 (2015), 725–738.
53. Siegel, R.L., Miller, K.D., Jemal, A., Cancer statistics, 2018. CA Cancer J. Clin. 68 (2018), 7–30.
54. Tibshiranin, R., Regression shrinkage and selection via Lasso. J. R. Statist. Soc 58 (1996), 267–288.
55. Vétizou, M., Pitt, J.M., Daillère, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M.P., Duong, C.P., et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350 (2015), 1079–1084.
56. Vogelstein, B., Papadopoulos, N., Velculescu, V.E., Zhou, S., Diaz, L.A. Jr., Kinzler, K.W., Cancer genome landscapes. Science 339 (2013), 1546–1558.
57. Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73 (2007), 5261–5267.