Probiotic treatment reduces appetite and glucose level in the zebrafish model

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Falcinelli, Silvia ^a   Rodiles, Ana ^b   Unniappan, Suraj ^c   Picchietti, Simona ^d   Gioacchini, Giorgia ^a   Merrifield, Daniel Lee ^b   Carnevali, Oliana ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d UNIVERSITY OF TUSCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; GLUCOSE; PROBIOTIC AGENT;

ANIMAL; APPETITE; GASTROINTESTINAL ABSORPTION; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENETICS; INTESTINE FLORA; LARVA; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; ZEBRA FISH;

ANIMALS; APPETITE; FATTY ACIDS; GASTROINTESTINAL ABSORPTION; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; GENE EXPRESSION; GLUCOSE; LARVA; PROBIOTICS; ZEBRAFISH;

EID: 84953279235     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep18061     Document Type: Article

References (68)

1. Cani, P. D. & Delzenne, N. M. The role of the gut microbiota in energy metabolism and metabolic disease. Curr. Pharm. Des. 15, 1546-1558 (2009).
2. Falcinelli, S. et al. Lactobacillus rhamnosus lowers zebrafish lipid content by changing gut microbiota and host transcription of genes involved in lipid metabolism. Sci. Rep. 5 (2015).
3. Guinane, C. M. & Cotter, P. D. Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap. Adv. Gastroenterol. 6, 295-308 (2013).
4. Jumpertz, R. et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 94, 58-65 (2011).
5. Sonnenburg, J. L. & Fischbach, M. A. Community health care: therapeutic opportunities in the human microbiome. Sci. Transl. Med. 3, 78ps12-78ps12 (2011).
6. Greiner, T. U., Hyötyläinen, T., Knip, M., Bäckhed, F. & Ore͉i, M. The gut microbiota modulates glycaemic control and serum metabolite profiles in non-obese diabetic mice. PLoS ONE. doi: 10.1371/journal.pone.0110359 (2014).
7. Dobson, A. J. et al. Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster. Nat. Commun. doi: 10.1038/ncomms7312 (2015).
8. Chaston, J. M., Newell, P. D. & Douglas, A. E. Metagenome-wide association of microbial determinants of host phenotype in Drosophila melanogaster. mBio 5, e01631-01614 (2014).
9. Mojsov, S. Glucagon-like peptide-1 (GLP-1) and the control of glucose metabolism in mammals and teleost fish. Am. Zool. 40, 246-258 (2000).
10. Karnani, M. & Burdakov, D. Multiple hypothalamic circuits sense and regulate glucose levels. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R47-R55 (2011).
11. Dhillo, W. S. Appetite regulation: an overview. Thyroid 17, 433-445 (2007).
12. Liu, Q. et al. Expression of leptin receptor gene in developing and adult zebrafish. Gen. Comp. Endocrinol. 166, 346-355 (2010).
13. Zhang, Y. et al. Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432 (1994).
14. Bado, A. et al. The stomach is a source of leptin. Nature 394, 790-793 (1998).
15. Johnson, R. M., Johnson, T. M. & Londraville, R. L. Evidence for leptin expression in fishes. J. Exp. Zool. 286, 718 (2000).
16. Baicy, K. et al. Leptin replacement alters brain response to food cues in genetically leptin-deficient adults. Proc. Natl. Acad. Sci. USA 104, 18276-18279 (2007).
17. Muraoka, O. et al. Leptin-induced transactivation of NPY gene promoter mediated by JAK1, JAK2 and STAT3 in the neural cell lines. Neurochem. Int. 42, 591-601 (2003).
18. Di Marzo, V. et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410, 822-825 (2001).
19. Itoh, M. et al. Melanocortin 4 Receptor-Deficient Mice as a Novel Mouse Model of Nonalcoholic Steatohepatitis. Am. J. Pathol. 179, 2454-2463 (2011).
20. Huszar, D. et al. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88, 131-141 (1997).
21. Vaisse, C., Clement, K., Guy-Grand, B. & Froguel, P. A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat. Genet. 20, 113-114 (1998).
22. Osei-Hyiaman, D., Harvey-White, J., Batkai, S. & Kunos, G. The role of the endocannabinoid system in the control of energy homeostasis. Int. J. Obesity 30, S33-S38 (2006).
23. Pai, W.-Y. et al. Cannabinoid receptor 1 promotes hepatic lipid accumulation and lipotoxicity through the induction of SREBP-1c expression in zebrafish. Transgenic Res. 22, 823-838 (2013).
24. Zhang, L. et al. Peripheral neuropeptide Y Y1 receptors regulate lipid oxidation and fat accretion. Int. J. Obesity 34, 357-373 (2009).
25. Marks, J. L. & Waite, K. Intracerebroventricular neuropeptide Y acutely influences glucose metabolism and insulin sensitivity in the rat. J. Neuroendocrinol. 9, 99-103 (1997).
26. Rosmaninho-Salgado, J. et al. Intracellular mechanisms coupled to NPY Y 2 and Y 5 receptor activation and lipid accumulation in murine adipocytes. Neuropeptides 46(6), 359-366 (2012).
27. Oh-I, S. et al. Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature 443, 709-712 (2006).
28. Shimizu, H. & Osaki, A. Nesfatin/Nucleobindin-2 (NUCB2) and Glucose Homeostasis. Curr. Hypertens. Rev. 9(4), 270-273 (2014).
29. Mohan, H. & Unniappan, S. Phylogenetic aspects of nucleobindin-2/nesfatin-1. Curr. Pharm. Des. 19, 6929-6934 (2013).
30. Li, Z., Li, Y. & Zhang, W. Regulation of glucose metabolism by nesfatin-1. FASEB J. 27, 1160.1162 (2013).
31. Lim, G. E. & Brubaker, P. L. Glucagon-like peptide 1 secretion by the L-cell the view from within. Diabetes 55, S70-S77 (2006).
32. Elo, B., Villano, C., Govorko, D. & White, L. Larval zebrafish as a model for glucose metabolism: expression of phosphoenolpyruvate carboxykinase as a marker for exposure to anti-diabetic compounds. J. Mol. Endocrinol. 38, 433-440 (2007).
33. Gnügge, L., Meyer, D. & Driever, W. Pancreas development in zebrafish. Methods Cell Biol. 76, 531-551 (2003).
34. Yang, J., Brown, M. S., Liang, G., Grishin, N. V. & Goldstein, J. L. Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell 132, 387-396 (2008).
35. Shlimun, A. & Unniappan, S. Ghrelin O-Acyl transferase: bridging ghrelin and energy homeostasis. Int. J. Pept. doi: org/10.1155/2011/217957 (2011).
36. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200 (2011).
37. Bray, J. R. & Curtis, J. T. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27, 325-349 (1957).
38. Lozupone, C. A., Hamady, M., Kelley, S. T. & Knight, R. Quantitative and qualitative ? diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576-1585 (2007).
39. Mohan, H. & Unniappan, S. Discovery of ghrelin O-Acyltransferase. Endocr. Dev. 25, 16-24 (2013).
40. Balthasar, N. et al. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123, 493-505 (2005).
41. Di Marzo, V. & Matias, I. Endocannabinoid control of food intake and energy balance. Nat. Neurosci. 8, 585-589 (2005).
42. Bergen, H. T., Mizuno, T., Taylor, J. & Mobbs, C. V. Resistance to diet-induced obesity is associated with increased proopiomelanocortin mRNA and decreased neuropeptide Y mRNA in the hypothalamus. Brain Res. 851, 198-203 (1999).
43. Donohoe, D. R. et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell metab. 13, 517-526 (2011).
44. Hooper, L. V., Midtvedt, T. & Gordon, J. I. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22, 283-307 (2002).
45. Gioacchini, G. et al. Interplay between autophagy and apoptosis in the development of Danio rerio follicles and the effects of a probiotic. Reprod. Fertil. Dev. 25, 1115-1125 (2013).
46. Sobhani, I. et al. Leptin secretion and leptin receptor in the human stomach. Gut 47, 178-183 (2000).
47. Price, C. J., Samson, W. K. & Ferguson, A. V. Nesfatin-1 inhibits NPY neurons in the arcuate nucleus. Brain Res. 1230, 99-106 (2008).
48. Zhao, T.-J. et al. Ghrelin O-Acyltransferase (GOAT) is essential for growth hormone-mediated survival of calorie-restricted mice. Proc. Natl. Acad. Sci. USA 107, 7467-7472 (2010).
49. Kirchner, H. et al. GOAT links dietary lipids with the endocrine control of energy balance. Nat. Med. 15, 741-745 (2009).
50. Ogawa, J. et al. Production of conjugated fatty acids by lactic acid bacteria. J. Biosci. Bioeng. 100, 355-364 (2005).
51. Schlegel, A. & Stainier, D. Y. Microsomal triglyceride transfer protein is required for yolk lipid utilization and absorption of dietary lipids in zebrafish larvae. Biochemistry 45, 15179-15187 (2006).
52. Otis, J. P. & Farber, S. A. Imaging vertebrate digestive function and lipid metabolism in vivo. Drug. Discov. Today Dis. Models 10, e11-e16 (2013).
53. Dailey, M. J. & Moran, T. H. Glucagon-like peptide 1 and appetite. Trends Endocrinol. Metab. 24, 85-91 (2013).
54. Yadav, H., Lee, J.-H., Lloyd, J., Walter, P. & Rane, S. G. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J. Biol. Chem. 288, 25088-25097 (2013).
55. Gross, D. A., Zhan, C. & Silver, D. L. Direct binding of triglyceride to fat storage-inducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proc. Natl. Acad. Sci. USA 108, 19581-19586 (2011).
56. Semova, I. et al. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 12, 277-288 (2012).
57. Standen, B. et al. Modulation of the intestinal microbiota and morphology of tilapia, Oreochromis niloticus, following the application of a multi-species probiotic. Appl. Microbiol. Biotechnol. 1-15 (2015).
58. Roeselers, G. et al. Evidence for a core gut microbiota in the zebrafish. ISME J. 5, 1595-1608 (2011).
59. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
60. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
61. DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microb. 72, 5069-5072 (2006).
62. 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. Microb. 73, 5261-5267 (2007).
63. Caporaso, J. G. et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267 (2010).
64. Abrámoff, M. D., Magalhães, P. J. & Ram, S. J. Image processing with ImageJ. Biophotonics international 11, 36-42 (2004).
65. Maradonna, F. et al. Probiotic Supplementation Promotes Calcification in Danio rerio Larvae: A Molecular Study. PloS one 8, e83155 (2013).
66. McCurley, A. T. & Callard, G. V. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol. Biol. 9, 102 (2008).
67. Aursnes, I. A., Rishovd, A. L., Karlsen, H. E. & Gjøen, T. Validation of reference genes for quantitative RT-qPCR studies of gene expression in Atlantic cod (Gadus morhua l.) during temperature stress. BMC Res. Notes 4, 104 (2011).
68. Bustin, S. A. et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622 (2009).