Gut Microbe–Mediated Suppression of Inflammation-Associated Colon Carcinogenesis by Luminal Histamine Production

American Journal of Pathology

Volumn 187, Issue 10, 2017, Pages 2323-2336

  Gao, Chunxu ^a,b   Ganesh, Bhanu Priya ^a,b   Shi, Zhongcheng ^a,b   Shah, Rajesh Rasik ^a   Fultz, Robert ^a,b   Major, Angela ^b   Venable, Susan ^a,b   Lugo, Monica ^a,b   Hoch, Kathleen ^b   Chen, Xiaowei ^c   Haag, Anthony ^a,b   Wang, Timothy C ^c   Versalovic, James ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOATTRACTANT; FLUORODEOXYGLUCOSE F 18; HISTAMINE; HISTIDINE DECARBOXYLASE; INTERLEUKIN 1ALPHA; INTERLEUKIN 22; INTERLEUKIN 6; KERATINOCYTE CHEMOATTRACTANT; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CYTOKINE; HISTAMINE H2 RECEPTOR; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL COUNT; COLITIS; COLON CANCER; COLON CARCINOGENESIS; COLON MUCOSA; CONTROLLED STUDY; GENE EXPRESSION; HISTAMINE RELEASE; INTESTINE FLORA; LACTOBACILLUS REUTERI; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; TUMOR VOLUME; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; BIOSYNTHESIS; BLOOD; CARCINOGENESIS; COLORECTAL TUMOR; DIAGNOSTIC IMAGING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INFLAMMATION; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; SPLEEN; SURVIVAL ANALYSIS;

ANIMALS; CARCINOGENESIS; COLORECTAL NEOPLASMS; CYTOKINES; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTAMINE; HISTIDINE DECARBOXYLASE; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; LACTOBACILLUS REUTERI; MICE, INBRED BALB C; MODELS, BIOLOGICAL; MYELOID CELLS; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, HISTAMINE H2; RNA, MESSENGER; SPLEEN; SURVIVAL ANALYSIS;

EID: 85029178141     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2017.06.011     Document Type: Article

References (60)

1. Siegel, R., Desantis, C., Jemal, A., Colorectal cancer statistics, 2014. CA Cancer J Clin 64 (2014), 104–117.
2. Jess, T., Simonsen, J., Jorgensen, K.T., Pedersen, B.V., Nielsen, N.M., Frisch, M., Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years. Gastroenterology 143 (2012), 375–381.e1 quiz e13–e14.
3. Herrinton, L.J., Liu, L., Levin, T.R., Allison, J.E., Lewis, J.D., Velayos, F., Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010. Gastroenterology 143 (2012), 382–389.
4. Beaugerie, L., Svrcek, M., Seksik, P., Bouvier, A.M., Simon, T., Allez, M., Brixi, H., Gornet, J.M., Altwegg, R., Beau, P., Duclos, B., Bourreille, A., Faivre, J., Peyrin-Biroulet, L., Flejou, J.F., Carrat, F., CESAME Study Group. Risk of colorectal high-grade dysplasia and cancer in a prospective observational cohort of patients with inflammatory bowel disease. Gastroenterology 145 (2013), 166–175.e8.
5. Terzic, J., Grivennikov, S., Karin, E., Karin, M., Inflammation and colon cancer. Gastroenterology 138 (2010), 2101–2114.e5.
6. Louis, P., Hold, G.L., Flint, H.J., The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12 (2014), 661–672.
7. Sears, C.L., Garrett, W.S., Microbes, microbiota, and colon cancer. Cell Host Microbe 15 (2014), 317–328.
8. Schwabe, R.F., Jobin, C., The microbiome and cancer. Nat Rev Cancer 13 (2013), 800–812.
9. Tjalsma, H., Boleij, A., Marchesi, J.R., Dutilh, B.E., A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 10 (2012), 575–582.
10. Arthur, J.C., Perez-Chanona, E., Muhlbauer, M., Tomkovich, S., Uronis, J.M., Fan, T.J., Campbell, B.J., Abujamel, T., Dogan, B., Rogers, A.B., Rhodes, J.M., Stintzi, A., Simpson, K.W., Hansen, J.J., Keku, T.O., Fodor, A.A., Jobin, C., Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338 (2012), 120–123.
11. Arthur, J.C., Gharaibeh, R.Z., Muhlbauer, M., Perez-Chanona, E., Uronis, J.M., McCafferty, J., Fodor, A.A., Jobin, C., Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun, 5, 2014, 4724.
12. Goodwin, A.C., Destefano Shields, C.E., Wu, S., Huso, D.L., Wu, X., Murray-Stewart, T.R., Hacker-Prietz, A., Rabizadeh, S., Woster, P.M., Sears, C.L., Casero, R.A. Jr., Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci U S A 108 (2011), 15354–15359.
13. Rowland, I.R., Rumney, C.J., Coutts, J.T., Lievense, L.C., Effect of Bifidobacterium longum and inulin on gut bacterial metabolism and carcinogen-induced aberrant crypt foci in rats. Carcinogenesis 19 (1998), 281–285.
14. Chen, C.C., Lin, W.C., Kong, M.S., Shi, H.N., Walker, W.A., Lin, C.Y., Huang, C.T., Lin, Y.C., Jung, S.M., Lin, T.Y., Oral inoculation of probiotics Lactobacillus acidophilus NCFM suppresses tumour growth both in segmental orthotopic colon cancer and extra-intestinal tissue. Br J Nutr 107 (2012), 1623–1634.
15. Verma, A., Shukla, G., Probiotics Lactobacillus rhamnosus GG, Lactobacillus acidophilus suppresses DMH-induced procarcinogenic fecal enzymes and preneoplastic aberrant crypt foci in early colon carcinogenesis in Sprague Dawley rats. Nutr Cancer 65 (2013), 84–91.
16. Casas, I.A., Dobrogosz, W.J., Validation of the probiotic concept: Lactobacillus reuteri confers broad-spectrum protection against disease in humans and animals. Microb Ecol Health Dis 12 (2000), 247–285.
17. Liu, Y., Fatheree, N.Y., Mangalat, N., Rhoads, J.M., Human-derived probiotic Lactobacillus reuteri strains differentially reduce intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 299 (2010), G1087–G1096.
18. Thomas, C.M., Hong, T., van Pijkeren, J.P., Hemarajata, P., Trinh, D.V., Hu, W., Britton, R.A., Kalkum, M., Versalovic, J., Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One, 7, 2012, e31951.
19. Madsen, K.L., Doyle, J.S., Jewell, L.D., Tavernini, M.M., Fedorak, R.N., Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116 (1999), 1107–1114.
20. Pena, J.A., Li, S.Y., Wilson, P.H., Thibodeau, S.A., Szary, A.J., Versalovic, J., Genotypic and phenotypic studies of murine intestinal lactobacilli: species differences in mice with and without colitis. Appl Environ Microbiol 70 (2004), 558–568.
21. Schreiber, O., Petersson, J., Phillipson, M., Perry, M., Roos, S., Holm, L., Lactobacillus reuteri prevents colitis by reducing P-selectin-associated leukocyte- and platelet-endothelial cell interactions. Am J Physiol Gastrointest Liver Physiol 296 (2009), G534–G542.
22. Preidis, G.A., Saulnier, D.M., Blutt, S.E., Mistretta, T.A., Riehle, K.P., Major, A.M., Venable, S.F., Barrish, J.P., Finegold, M.J., Petrosino, J.F., Guerrant, R.L., Conner, M.E., Versalovic, J., Host response to probiotics determined by nutritional status of rotavirus-infected neonatal mice. J Pediatr Gastroenterol Nutr 55 (2012), 299–307.
23. Gao, C., Major, A., Rendon, D., Lugo, M., Jackson, V., Shi, Z., Mori-Akiyama, Y., Versalovic, J., Histamine H2 receptor-mediated suppression of intestinal inflammation by probiotic Lactobacillus reuteri. MBio, 6, 2015, e01358-15.
24. Spinler, J., Sontakke, A., Hollister, E., Venable, S., Oh, L.P., Balderas, M., Saulnier, D.M.A., Mistretta, T.A., Devaraj, S., Walter, J., Versalovic, J., Highlander, S.K., From prediction to function using evolutionary genomics: human-specific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol Evol 6 (2014), 1772–1789.
25. Preidis, G.A., Versalovic, J., Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136 (2009), 2015–2031.
26. Hemarajata, P., Gao, C., Pflughoeft, K.J., Thomas, C.M., Saulnier, D.M., Spinler, J.K., Versalovic, J., Lactobacillus reuteri-specific immunoregulatory gene rsiR modulates histamine production and immunomodulation by Lactobacillus reuteri. J Bacteriol 195 (2013), 5567–5576.
27. Yang, X.D., Ai, W., Asfaha, S., Bhagat, G., Friedman, R.A., Jin, G., Park, H., Shykind, B., Diacovo, T.G., Falus, A., Wang, T.C., Histamine deficiency promotes inflammation-associated carcinogenesis through reduced myeloid maturation and accumulation of CD11b+Ly6G+ immature myeloid cells. Nat Med 17 (2011), 87–95.
28. Goswami, C.P., Nakshatri, H., PROGgeneV2: enhancements on the existing database. BMC Cancer, 14, 2014, 970.
29. Preidis, G.A., Saulnier, D.M., Blutt, S.E., Mistretta, T.A., Riehle, K.P., Major, A.M., Venable, S.F., Finegold, M.J., Petrosino, J.F., Conner, M.E., Versalovic, J., Probiotics stimulate enterocyte migration and microbial diversity in the neonatal mouse intestine. FASEB J 26 (2012), 1960–1969.
30. Ganesh, B.P., Richter, J.F., Blaut, M., Loh, G., Enterococcus faecium NCIMB 10415 does not protect interleukin-10 knock-out mice from chronic gut inflammation. Benef Microbes 3 (2012), 43–50.
31. Landskron, G., De la Fuente, M., Thuwajit, P., Thuwajit, C., Hermoso, M.A., Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res, 2014, 2014, 149185.
32. Sander, L.E., Lorentz, A., Sellge, G., Coeffier, M., Neipp, M., Veres, T., Frieling, T., Meier, P.N., Manns, M.P., Bischoff, S.C., Selective expression of histamine receptors H1R, H2R, and H4R, but not H3R, in the human intestinal tract. Gut 55 (2006), 498–504.
33. Ferstl, R., Frei, R., Schiavi, E., Konieczna, P., Barcik, W., Ziegler, M., Lauener, R.P., Chassard, C., Lacroix, C., Akdis, C.A., O'Mahony, L., Histamine receptor 2 is a key influence in immune responses to intestinal histamine-secreting microbes. J Allergy Clin Immunol 134 (2014), 744–746.e3.
34. Funaki, C., Hodges, R.R., Dartt, D.A., Identification of the Raf-1 signaling pathway used by cAMP to inhibit p42/p44 MAPK in rat lacrimal gland acini: role in potentiation of protein secretion. Invest Ophthalmol Vis Sci 51 (2010), 6321–6328.
35. Hershenson, M.B., Chao, T.S., Abe, M.K., Gomes, I., Kelleher, M.D., Solway, J., Rosner, M.R., Histamine antagonizes serotonin and growth factor-induced mitogen-activated protein kinase activation in bovine tracheal smooth muscle cells. J Biol Chem 270 (1995), 19908–19913.
36. Waltereit, R., Weller, M., Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol Neurobiol 27 (2003), 99–106.
37. Yamada, S., Guo, X., Wang, K.Y., Tanimoto, A., Sasaguri, Y., Novel function of histamine signaling via histamine receptors in cholesterol and bile acid metabolism: histamine H2 receptor protects against nonalcoholic fatty liver disease. Pathol Int 66 (2016), 376–385.
38. Wouters, M.M., Balemans, D., Van Wanrooy, S., Dooley, J., Cibert-Goton, V., Alpizar, Y.A., Valdez-Morales, E.E., Nasser, Y., Van Veldhoven, P.P., Vanbrabant, W., Van der Merwe, S., Mols, R., Ghesquiere, B., Cirillo, C., Kortekaas, I., Carmeliet, P., Peetermans, W.E., Vermeire, S., Rutgeerts, P., Augustijns, P., Hellings, P.W., Belmans, A., Vanner, S., Bulmer, D.C., Talavera, K., Vanden Berghe, P., Liston, A., Boeckxstaens, G.E., Histamine receptor H1-mediated sensitization of TRPV1 mediates visceral hypersensitivity and symptoms in patients with irritable Bowel syndrome. Gastroenterology 150 (2016), 875–887.e9.
39. Oquendo, P., Alberta, J., Wen, D.Z., Graycar, J.L., Derynck, R., Stiles, C.D., The platelet-derived growth factor-inducible KC gene encodes a secretory protein related to platelet alpha-granule proteins. J Biol Chem 264 (1989), 4133–4137.
40. Asfaha, S., Dubeykovskiy, A.N., Tomita, H., Yang, X., Stokes, S., Shibata, W., Friedman, R.A., Ariyama, H., Dubeykovskaya, Z.A., Muthupalani, S., Ericksen, R., Frucht, H., Fox, J.G., Wang, T.C., Mice that express human interleukin-8 have increased mobilization of immature myeloid cells, which exacerbates inflammation and accelerates colon carcinogenesis. Gastroenterology 144 (2013), 155–166.
41. Lee, Y.S., Choi, I., Ning, Y., Kim, N.Y., Khatchadourian, V., Yang, D., Chung, H.K., Choi, D., LaBonte, M.J., Ladner, R.D., Nagulapalli Venkata, K.C., Rosenberg, D.O., Petasis, N.A., Lenz, H.J., Hong, Y.K., Interleukin-8 and its receptor CXCR2 in the tumour microenvironment promote colon cancer growth, progression and metastasis. Br J Cancer 106 (2012), 1833–1841.
42. Fukui, H., Zhang, X., Sun, C., Hara, K., Kikuchi, S., Yamasaki, T., Kondo, T., Tomita, T., Oshima, T., Watari, J., Imura, J., Fujimori, T., Sasako, M., Miwa, H., IL-22 produced by cancer-associated fibroblasts promotes gastric cancer cell invasion via STAT3 and ERK signaling. Br J Cancer 111 (2014), 763–771.
43. Ji, Y., Yang, X., Li, J., Lu, Z., Li, X., Yu, J., Li, N., IL-22 promotes the migration and invasion of gastric cancer cells via IL-22R1/AKT/MMP-9 signaling. Int J Clin Exp Pathol 7 (2014), 3694–3703.
44. Kryczek, I., Lin, Y., Nagarsheth, N., Peng, D., Zhao, L., Zhao, E., Vatan, L., Szeliga, W., Dou, Y., Owens, S., Zgodzinski, W., Majewski, M., Wallner, G., Fang, J., Huang, E., Zou, W., IL-22(+)CD4(+) T cells promote colorectal cancer stemness via STAT3 transcription factor activation and induction of the methyltransferase DOT1L. Immunity 40 (2014), 772–784.
45. Rokavec, M., Oner, M.G., Li, H., Jackstadt, R., Jiang, L., Lodygin, D., Kaller, M., Horst, D., Ziegler, P.K., Schwitalla, S., Slotta-Huspenina, J., Bader, F.G., Greten, F.R., Hermeking, H., IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest 124 (2014), 1853–1867.
46. Waldner, M.J., Foersch, S., Neurath, M.F., Interleukin-6–a key regulator of colorectal cancer development. Int J Biol Sci 8 (2012), 1248–1253.
47. Nagasaki, T., Hara, M., Nakanishi, H., Takahashi, H., Sato, M., Takeyama, H., Interleukin-6 released by colon cancer-associated fibroblasts is critical for tumour angiogenesis: anti-interleukin-6 receptor antibody suppressed angiogenesis and inhibited tumour-stroma interaction. Br J Cancer 110 (2014), 469–478.
48. West, N.R., McCuaig, S., Franchini, F., Powrie, F., Emerging cytokine networks in colorectal cancer. Nat Rev Immunol 15 (2015), 615–629.
49. Watanabe, S., Deguchi, K., Zheng, R., Tamai, H., Wang, L.X., Cohen, P.A., Shu, S., Tumor-induced CD11b+Gr-1+ myeloid cells suppress T cell sensitization in tumor-draining lymph nodes. J Immunol 181 (2008), 3291–3300.
50. Kennedy, L., Hodges, K., Meng, F., Alpini, G., Francis, H., Histamine and histamine receptor regulation of gastrointestinal cancers. Transl Gastrointest Cancer 1 (2012), 215–227.
51. Cianchi, F., Vinci, M.C., Masini, E., Histamine in cancer: the dual faces of the coin. Cancer Biol Ther 7 (2008), 36–37.
52. Garcia-Caballero, M., Neugebauer, E., Campos, R., Nunez de Castro, I., Vara-Thorbeck, C., Increased histidine decarboxylase (HDC) activity in human colorectal cancer: results of a study on ten patients. Agents Actions 23 (1988), 357–360.
53. Borges-Canha, M., Portela-Cidade, J.P., Dinis-Ribeiro, M., Leite-Moreira, A.F., Pimentel-Nunes, P., Role of colonic microbiota in colorectal carcinogenesis: a systematic review. Rev Esp Enferm Dig 107 (2015), 659–671.
54. Mira-Pascual, L., Cabrera-Rubio, R., Ocon, S., Costales, P., Parra, A., Suarez, A., Moris, F., Rodrigo, L., Mira, A., Collado, M.C., Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. J Gastroenterol 50 (2015), 167–179.
55. O'Keefe, S.J., Chung, D., Mahmoud, N., Sepulveda, A.R., Manafe, M., Arch, J., Adada, H., van der Merwe, T., Why do African Americans get more colon cancer than Native Africans?. J Nutr 137 (2007), 175S–182S.
56. Moore, W.E., Moore, L.H., Intestinal floras of populations that have a high risk of colon cancer. Appl Environ Microbiol 61 (1995), 3202–3207.
57. Amirian, E.S., Zhou, R., Wrensch, M.R., Olson, S.H., Scheurer, M.E., Il'yasova, D., Lachance, D., Armstrong, G.N., McCoy, L.S., Lau, C.C., Claus, E.B., Barnholtz-Sloan, J.S., Schildkraut, J., Ali-Osman, F., Sadetzki, S., Johansen, C., Houlston, R.S., Jenkins, R.B., Bernstein, J.L., Merrell, R.T., Davis, F.G., Lai, R., Shete, S., Amos, C.I., Melin, B.S., Bondy, M.L., Approaching a scientific consensus on the association between allergies and glioma risk: a report from the Glioma International Case-Control Study. Cancer Epidemiol Biomarkers Prev 25 (2016), 282–290.
58. Negri, E., Bosetti, C., La Vecchia, C., Levi, F., Tomei, F., Franceschi, S., Allergy and other selected diseases and risk of colorectal cancer. Eur J Cancer 35 (1999), 1838–1841.
59. Prizment, A.E., Folsom, A.R., Cerhan, J.R., Flood, A., Ross, J.A., Anderson, K.E., History of allergy and reduced incidence of colorectal cancer, Iowa Women's Health Study. Cancer Epidemiol Biomarkers Prev 16 (2007), 2357–2362.
60. Barcik, W., Pugin, B., Westermann, P., Perez, N.R., Ferstl, R., Wawrzyniak, M., Smolinska, S., Jutel, M., Hessel, E.M., Michalovich, D., Akdis, C.A., Frei, R., O'Mahony, L., Histamine-secreting microbes are increased in the gut of adult asthma patients. J Allergy Clin Immunol 138 (2016), 1491–1494.e7.