Cadaverine, a metabolite of the microbiome, reduces breast cancer aggressiveness through trace amino acid receptors

Scientific Reports

Volumn 9, Issue 1, 2019, Pages

  Kovács, Tünde ^a   Mikó, Edit ^a,b   Vida, András ^a,b   Sebő, Éva ^c   Toth, Judit ^a   Csonka, Tamás ^a   Boratkó, Anita ^a   Ujlaki, Gyula ^a   Lente, Gréta ^a   Kovács, Patrik ^a   Tóth, Dezső ^a   Árkosy, Péter ^a   Kiss, Borbála ^a   Méhes, Gábor ^a   Goedert, James J ^d   Bai, Péter ^a,b  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b MTA DE Lendulet Laboratory of Cellular Metabolism   (Hungary)

^c Kenezy Korhaz Rendelointezet   (Hungary)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RECEPTOR; CADAVERINE;

BIOLOGICAL MODEL; BREAST TUMOR; CELL MOTION; CELL PROLIFERATION; DISEASE EXACERBATION; DRUG EFFECT; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; KAPLAN MEIER METHOD; METABOLISM; MICROFLORA; MORTALITY; PATHOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CADAVERINE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; MICROBIOTA; MODELS, BIOLOGICAL; RECEPTORS, AMINO ACID;

EID: 85061046595     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-37664-7     Document Type: Article

References (69)

1. Macfabe, D. Autism: metabolism, mitochondria, and the microbiome. Glob Adv Health Med 2, 52–66 (2013)
2. Maruvada, P., Leone, V., Kaplan, L. M. & Chang, E. B. The Human Microbiome and Obesity: Moving beyond Associations. Cell Host Microbe. 22, 589–599 (2017)
3. Fulbright, L. E., Ellermann, M. & Arthur, J. C. The microbiome and the hallmarks of cancer. PLoS Pathog. 13, e1006480 (2017)
4. Kundu, P., Blacher, E., Elinav, E. & Pettersson, S. Our Gut Microbiome: The Evolving Inner Self. Cell. 171, 1481–1493, 10.1016/j.cell.2017.1411.1024. (2017)
5. Zitvogel, L., Ayyoub, M., Routy, B. & Kroemer, G. Microbiome and Anticancer Immunosurveillance. Cell. 165, 276–287, 10.1016/j.cell.2016.1003.1001. (2016)
6. Schwabe, R. F. & Jobin, C. The microbiome and cancer. Nat Rev Cancer 13, 800–812 (2013)
7. Plottel, C. S. & Blaser, M. J. Microbiome and malignancy. Cell Host Microbe 10, 324–335 (2011)
8. Garrett, W. S. Cancer and the microbiota. Science. 348, 80–86 (2015)
9. Yu, H. et al. Urinary microbiota in patients with prostate cancer and benign prostatic hyperplasia. Archives of medical science: AMS 11, 385–394 (2015)
10. Chase, D., Goulder, A., Zenhausern, F., Monk, B. & Herbst-Kralovetz, M. The vaginal and gastrointestinal microbiomes in gynecologic cancers: a review of applications in etiology, symptoms and treatment. Gynecol Oncol 138, 190–200 (2015)
11. Yu, Y., Champer, J., Beynet, D., Kim, J. & Friedman, A. J. The role of the cutaneous microbiome in skin cancer: lessons learned from the gut. Journal of drugs in dermatology: JDD 14, 461–465 (2015)
12. Gui, Q. F., Lu, H. F., Zhang, C. X., Xu, Z. R. & Yang, Y. H. Well-balanced commensal microbiota contributes to anti-cancer response in a lung cancer mouse model. Genetics and molecular research: GMR 14, 5642–5651 (2015)
13. Yamamoto, M. L. & Schiestl, R. H. Lymphoma caused by intestinal microbiota. International journal of environmental research and public health 11, 9038–9049 (2014)
14. Yamamoto, M. L. & Schiestl, R. H. Intestinal microbiome and lymphoma development. Cancer J. 20, 190–194 (2014)
15. Goedert, J. J. et al. Postmenopausal breast cancer and oestrogen associations with the IgA-coated and IgA-noncoated faecal microbiota. Br J Cancer 23, 435 (2018)
16. Goedert, J. J. et al. Investigation of the association between the fecal microbiota and breast cancer in postmenopausal women: a population-based case-control pilot study. J Natl Cancer Inst. 107, djv147 (2015)
17. Fuhrman, B. J. et al. Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women. J Clin Endocrinol Metab. 99, 4632–4640 (2014)
18. Flores, R. et al. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: a cross-sectional study. J Transl Med. 10, 253 (2012)
19. Xuan, C. et al. Microbial dysbiosis is associated with human breast cancer. PLoS One. 9, e83744 (2014)
20. Hieken, T. J. et al. The Microbiome of Aseptically Collected Human Breast Tissue in Benign and Malignant Disease. Sci Rep. 6, 30751 (2016)
21. Chan, A. A. et al. Characterization of the microbiome of nipple aspirate fluid of breast cancer survivors. Sci Rep. 6, 28061 (2016)
22. Urbaniak, C. et al. The Microbiota of Breast Tissue and Its Association with Breast Cancer. Appl Environ Microbiol. 82, 5039–5048 (2016)
23. Yoshimoto, S. et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 499, 97–101 (2013)
24. Xie, G. et al. Dysregulated hepatic bile acids collaboratively promote liver carcinogenesis. Int J Cancer. 139, 1764–1775 (2016)
25. Luu, T. H. et al. Lithocholic bile acid inhibits lipogenesis and induces apoptosis in breast cancer cells. Cell Oncol (Dordr). 41, 13–24 (2018)
26. Miko, E. et al. Lithocholic acid, a bacterial metabolite reduces breast cancer cell proliferation and aggressiveness. Biochim Biophys Acta 1859, 958–974 (2018)
27. Rowland, I. R. Role of the gut flora in toxicity and cancer (Academic Press, Carshalton, UK, 1988)
28. Shellman, Z. et al. Bile acids: a potential role in the pathogenesis of pharyngeal malignancy. Clin Otolaryngol. 42, 969–973 (2017)
29. Dapito, D. H. et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 21, 504–516 (2012)
30. Bindels, L. B. et al. Gut microbiota-derived propionate reduces cancer cell proliferation in the liver. Br J Cancer 107, 1337–1344 (2012)
31. Miller-Fleming, L., Olin-Sandoval, V., Campbell, K. & Ralser, M. Remaining Mysteries of Molecular Biology: The Role of Polyamines in the Cell. J Mol Biol. 427, 3389–3406 (2015)
32. Seiler, N. Catabolism of polyamines. Amino Acids. 26, 217–233 (2004)
33. Loser, C., Folsch, U. R., Paprotny, C. & Creutzfeldt, W. Polyamine concentrations in pancreatic tissue, serum, and urine of patients with pancreatic cancer. Pancreas. 5, 119–127 (1990)
34. Loser, C., Folsch, U. R., Paprotny, C. & Creutzfeldt, W. Polyamines in colorectal cancer. Evaluation of polyamine concentrations in the colon tissue, serum, and urine of 50 patients with colorectal cancer. Cancer. 65, 958–966 (1990)
35. Pavlides, S. et al. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell Cycle 8, 3984–4001 (2009)
36. Liberles, S. D. Trace amine-associated receptors: ligands, neural circuits, and behaviors. Curr Opin Neurobiol. 34, 1–7 (2015)
37. Vattai, A. et al. Increased trace amine-associated receptor 1 (TAAR1) expression is associated with a positive survival rate in patients with breast cancer. J Cancer Res Clin Oncol 13, 017–2420 (2017)
38. NCBI_GEO_Profiles. TAAR8 expression in hyperplastic enlarged lubular units (HELUs) versus normal terminal ductal lobular units (TDLUs). (https://www.ncbi.nlm.nih.gov/geoprofiles/39407988, 2018)
39. Gent_Database. TAAR8 expression in cancers (search term: TAAR8). (http://medicalgenome.kribb.re.kr/GENT/ 2018)
40. NCBI_GEO_Profiles. TAAR8 expression in DCIS vs. healthy breast tissue. (https://www.ncbi.nlm.nih.gov/geo/tools/profileGraph.cgi?ID=GDS3853:1553552_at, 2018)
41. NCBI_GEO_Profiles. TAAR8 - Invasive ductal and lobular breast carcinomas. (https://www.ncbi.nlm.nih.gov/geoprofiles/36691448, 2018)
42. NCBI_GEO_Profiles. LDC expression in control, DCIS, ICS. Vol. 2018 (https://www.ncbi.nlm.nih.gov/geo/tools/profileGraph.cgi?ID=GDS3853:201744_s_at, 2018)
43. NCBI_GEO_Profiles. LDC expression in epithelium and stroma of normal breast and invasive breast cancer. Vol. 2018 (https://www.ncbi.nlm.nih.gov/geo/tools/profileGraph.cgi?ID=GDS3324:201744_s_at, 2018)
44. NCBI_GEO_Profiles. LDC expression in ER− and ER+ breast cancer patients, prophylactic mastectomy patients, and normal breast epithelia from reduction mammoplasty patients., Vol. 2018 (https://www.ncbi.nlm.nih.gov/geo/tools/profileGraph.cgi?ID=GDS3716:201744_s_at, 2018)
45. NCBI_GEO_Profiles. Normal epithelium vs. breast cancer epithelium in patients. (https://www.ncbi.nlm.nih.gov/geo/tools/profileGraph.cgi?ID=GDS3139:201744_s_at, 2018)
46. NCBI_GEO_Profiles. LDC expression in control vs. non-basal vs. basal-like breast cancer. Vol. 2018 (https://www.ncbi.nlm.nih.gov/geo/tools/profileGraph.cgi?ID=GDS2250:201744_s_at, 2018)
47. Mashige, F. et al. Clinical usefulness of an enzymatic determination of total urinary polyamines, excluding cadaverine. Clin Chem. 34, 2271–2274 (1988)
48. Elitsur, Y., Moshier, J. A., Murthy, R., Barbish, A. & Luk, G. D. Polyamine levels, ornithine decarboxylase (ODC) activity, and ODC-mRNA expression in normal and cancerous human colonocytes. Life Sci 50, 1417–1424 (1992)
49. Khuhawar, M. Y. & Qureshi, G. A. Polyamines as cancer markers: applicable separation methods. J Chromatogr B Biomed Sci Appl. 764, 385–407 (2001)
50. Liu, R. et al. Determination of polyamine metabolome in plasma and urine by ultrahigh performance liquid chromatography-tandem mass spectrometry method: application to identify potential markers for human hepatic cancer. Anal Chim Acta. 791, 36–45 (2013)
51. Olaya, J., Neopikhanov, V. & Uribe, A. Lipopolysaccharide of Escherichia coli, polyamines, and acetic acid stimulate cell proliferation in intestinal epithelial cells. In Vitro Cell Dev Biol Anim. 35, 43–48 (1999)
52. Aizencang, G. et al. Antiproliferative effects of N1,N4-dibenzylputrescine in human and rodent tumor cells. Cell Mol Biol (Noisy-le-grand). 44, 615–625 (1998)
53. Velicer, C. M. et al. Antibiotic use in relation to the risk of breast cancer. JAMA. 291, 827–835 (2004)
54. Velicer, C. M., Heckbert, S. R., Rutter, C., Lampe, J. W. & Malone, K. Association between antibiotic use prior to breast cancer diagnosis and breast tumour characteristics (United States). Cancer Causes Control. 17, 307–313 (2006)
55. Friedman, G. D. et al. Antibiotics and risk of breast cancer: up to 9 years of follow-up of 2.1 million women. Cancer Epidemiol Biomarkers Prev. 15, 2102–2106 (2006)
56. Wirtz, H. S. et al. Frequent antibiotic use and second breast cancer events. Cancer Epidemiol Biomarkers Prev. 22, 1588–1599 (2013)
57. Tamim, H. M., Hanley, J. A., Hajeer, A. H., Boivin, J. F. & Collet, J. P. Risk of breast cancer in relation to antibiotic use. Pharmacoepidemiol Drug Saf. 17, 144–150 (2008)
58. Satram-Hoang, S. et al. A pilot study of male breast cancer in the Veterans Affairs healthcare system. J Environ Pathol Toxicol Oncol 29, 235–244 (2010)
59. Marton, J. et al. Poly(ADP-ribose) polymerase-2 is a lipid-modulated modulator of muscular lipid homeostasis. Biochim Biophys Acta 2, 30187–30182 (2018)
60. Fodor, T. et al. Combined Treatment of MCF-7 Cells with AICAR and Methotrexate, Arrests Cell Cycle and Reverses Warburg Metabolism through AMP-Activated Protein Kinase (AMPK) and FOXO1. PLoS One. 11, e0150232 (2016)
61. Robaszkiewicz, A. et al. Hydrogen peroxide-induced poly(ADP-ribosyl)ation regulates osteogenic differentiation-associated cell death. Free Radic Biol Med. 53, 1552–1564 (2012)
62. Nagy, L. et al. Glycogen phosphorylase inhibition improves beta cell function. Br J Pharmacol. 175, 301–319 (2018)
63. Szántó, M. et al. Deletion of PARP-2 induces hepatic cholesterol accumulation and decrease in HDL levels. Biochem Biophys Acta - Molecular Basis of Disease 1842, 594–602 (2014)
64. Mabley, J. G. et al. Suppression of intestinal polyposis in Apcmin/+ mice by targeting the nitric oxide or poly(ADP-ribose) pathways. Mutat.Res. 548, 107–116 (2004)
65. Fiorillo, M. et al. Bergamot natural products eradicate cancer stem cells (CSCs) by targeting mevalonate, Rho-GDI-signalling and mitochondrial metabolism. Biochim Biophys Acta 4, 30061–30066 (2018)
66. Kilkenny, C., Browne, W., Cuthill, I. C., Emerson, M. & Altman, D. G. NC3Rs Reporting Guidelines Working Group. Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol. 160 (7), 1577 – 1579 (2010)
67. McGrath, J. C., Drummond, G. B., McLachlan, E. M., Kilkenny, C. & Wainwright, C. L. Guidelines for reporting experiments involving animals: th e ARRIVE guidelines. Br J Pharmacol. 160(7), 1573–1576 (2010)
68. Nagy, G. G., Varvolgyi, C., Balogh, Z., Orosi, P. & Paragh, G. Detailed methodological recommendations for the treatment of Clostridium difficile-associated diarrhea with faecal transplantation. Orv Hetil. 154, 10–19 (2013)
69. Lanczky, A. et al. miRpower: a web-tool to validate survival-associated miRNAs utilizing expression data from 2178 breast cancer patients. Breast Cancer Res Treat. 160, 439–446 (2016)