Rett syndrome: A focus on gut microbiota

International Journal of Molecular Sciences

Volumn 18, Issue 2, 2017, Pages

  Borghi, Elisa ^a   Borgo, Francesca ^a   Severgnini, Marco ^b   Savini, Miriam Nella ^c   Casiraghi, Maria Cristina ^a   Vignoli, Aglaia ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c ASST Santi Paolo e Carlo University Hospital   (Italy)

Author keywords

Diet; Microbiota; Rett syndrome; Short chain fatty acids

Indexed keywords

BUTYRIC ACID; METHYL CPG BINDING PROTEIN 2; PROPIONIC ACID; SHORT CHAIN FATTY ACID;

ADULT; ARTICLE; BACTEROIDACEAE; CALORIC INTAKE; CLINICAL ARTICLE; CLOSTRIDIUM; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GAS CHROMATOGRAPHY; GENE MUTATION; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; HUMAN; INTESTINE FLORA; MACRONUTRIENT; PHENOTYPE; RETT SYNDROME; RUMINOCOCCACEAE; SUTTERELLA; YOUNG ADULT; ADOLESCENT; ALLELE; BACTERIUM; CLASSIFICATION; DIET; DYSBIOSIS; ENERGY METABOLISM; GENETICS; METABOLISM; MUTATION; RISK FACTOR; SEVERITY OF ILLNESS INDEX;

ADOLESCENT; ADULT; ALLELES; BACTERIA; DIET; DYSBIOSIS; ENERGY METABOLISM; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METHYL-CPG-BINDING PROTEIN 2; MUTATION; PHENOTYPE; RETT SYNDROME; RISK FACTORS; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

EID: 85011961693     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18020344     Document Type: Article

References (63)

1. Amir, R.E.; Van den Veyver, I.B.; Wan, M.; Tran, C.Q.; Francke, U.; Zoghbi, H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23, 185-188.
2. Marschik, P.B.; Kaufmann, W.E.; Sigafoos, J.; Wolin, T.; Zhang, D.; Bartl-Pokorny, K.D.; Pini, G.; Zappella, M.; Tager-Flusberg, H.; Einspieler, C et al. Changing the perspective on early development of Rett syndrome. Res. Dev. Disabil. 2013, 34, 1236-1239. [CrossRef] [PubMed]
3. Hagberg, B.; Romell, M. Rett females: Patterns of characteristic side-asymmetric neuroimpairments at long-term follow-up. Neuropediatrics 2002, 33, 324-326. [CrossRef] [PubMed]
4. Chahrour, M.; Zoghbi, H.Y. The story of rett syndrome: From clinic to neurobiology. Neuron 2007, 56, 422-437. [CrossRef] [PubMed]
5. Yasui, D.H.; Gonzales, M.L.; Aflatooni, J.O.; Crary, F.K.; Hu, D.J.; Gavino, B.J.; Golub, M.S.; Vincent, J.B.; Carolyn Schanen, N.; Olson, C.O et al. Mice with an isoform-ablating MECP2 exon 1 mutation recapitulate the neurologic deficits of Rett syndrome. Hum. Mol. Genet. 2014, 23, 2447-2458. [CrossRef] [PubMed]
6. Guy, J.; Cheval, H.; Selfridge, J.; Bird, A. The role of MeCP2 in the brain. Annu. Rev. Cell Dev. Biol. 2011, 27, 631-652. [CrossRef] [PubMed]
7. Yasui, D.H.; Peddada, S.; Bieda, M.C.; Vallero, R.O.; Hogart, A.; Nagarajan, R.P.; Thatcher, K.N.; Farnham, P.J.; Lasalle, J.M. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. USA 2007, 104, 19416-19421. [CrossRef] [PubMed]
8. Grillo, E.; Lo Rizzo, C.; Bianciardi, L.; Bizzarri, V.; Baldassarri, M.; Spiga, O.; Furini, S.; de Felice, C.; Signorini, C.; Leoncini, S et al. Revealing the complexity of a monogenic disease: Rett syndrome exome sequencing. PLoS ONE 2013, 8, e56599. [CrossRef] [PubMed]
9. Cuddapah, V.A.; Pillai, R.B.; Shekar, K.V.; Lane, J.B.; Motil, K.J.; Skinner, S.A.; Tarquinio, D.C.; Glaze, D.G.; McGwin, G.; Kaufmann, W.E et al. Methyl-CpG-binding protein 2 (MECP2) mutation type is associated with disease severity in Rett syndrome. J. Med. Genet. 2014, 51, 152-158. [CrossRef]
10. Wahba, G.; Schock, S.C.; Cudd, S.; Grynspan, D.; Humphreys, P.; Staines, W.A. Activity and MeCP2-dependent regulation of nNOS levels in enteric neurons. Neurogastroenterol. Motil. 2016, 28, 1723-1730. [CrossRef]
11. Symons, F.J.; Byiers, B.; Tervo, R.C.; Beisang, A. Parent-reported pain in Rett syndrome. Clin. J. Pain 2013, 29, 744-746. [CrossRef] [PubMed]
12. Strati, F.; Cavalieri, D.; Albanese, D.; de Felice, C.; Donati, C.; Hayek, J.; Jousson, O.; Leoncini, S.; Pindo, M.; Renzi, D et al. Altered gut microbiota in Rett syndrome. Microbiome 2016, 4, 41. [CrossRef] [PubMed]
13. Li, Q.; Zhou, J.M. The microbiota-gut-brain axis and its potential therapeutic role in autism spectrum disorder. Neuroscience 2016, 324, 131-139. [CrossRef]
14. Collins, S.M.; Surette, M.; Bercik, P. The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 2012, 10, 735-742. [CrossRef] [PubMed]
15. Rhee, S.H.; Pothoulakis, C.; Mayer, E.A. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 2009, 6, 306-314. [CrossRef] [PubMed]
16. Wong, J.M.; de Souza, R.; Kendall, C.W.; Emam, A.; Jenkins, D.J. Colonic health: Fermentation and short chain fatty acids. J. Clin. Gastroenterol. 2006, 40, 235-243. [CrossRef] [PubMed]
17. David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559-563. [CrossRef] [PubMed]
18. O'Keefe, S.J.; Li, J.V.; Lahti, L.; Ou, J.; Carbonero, F.; Mohammed, K.; Posma, J.M.; Kinross, J.; Wahl, E.; Ruder, E et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat. Commun. 2015, 6, 6342. [CrossRef] [PubMed]
19. Signorini, C.; de Felice, C.; Leoncini, S.; Durand, T.; Galano, J.M.; Cortelazzo, A.; Zollo, G.; Guerranti, R.; Gonnelli, S.; Caffarelli, C et al. Altered erythrocyte membrane fatty acid profile in typical Rett syndrome: Effects of !-3 polyunsaturated fatty acid supplementation. Prostaglandins Leukot. Essent. Fat. Acids 2014, 91, 183-193. [CrossRef] [PubMed]
20. Tabbaa, M.; Golubic, M.; Roizen, M.F.; Bernstein, A.M. Docosahexaenoic acid, inflammation, and bacterial dysbiosis in relation to periodontal disease, inflammatory bowel disease, and the metabolic syndrome. Nutrients 2013, 5, 3299-3310. [CrossRef] [PubMed]
21. Società Italiana di Nutrizione Umana (Italian Society of Human Nutrition, SINU). Nutrients and Energy Reference Intake Levels for Italian Population, 4th ed.; SICS: Milan, Italy, 2014.
22. Lewis, S.J.; Heaton, K.W. Stool form scale as a useful guide to intestinal transit time. Scand. J. Gastroenterol. 1997, 32, 920-924. [CrossRef] [PubMed]
23. Riva, A.; Borgo, F.; Lassandro, C.; Verduci, E.; Morace, G.; Borghi, E.; Berry, D. Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Env. Microbiol. 2016, 1-29. [CrossRef]
24. Vieira-Silva, S.; Falony, G.; Darzi, Y.; Lima-Mendez, G.; Garcia Yunta, R.; Okuda, S.; Vandeputte, D.; Valles-Colomer, M.; Hildebrand, F.; Chaffron, S et al. Species-function relationships shape ecological properties of the human gut microbiome. Nat. Microbiol. 2016, 124, 16088. [CrossRef] [PubMed]
25. Kang, D.W.; Park, J.G.; Ilhan, Z.E.; Wallstrom, G.; LaBaer, J.; Adams, J.B.; Krajmalnik-Brown, R. Reduced incidence of prevotella and other fermenters in intestinal microflora of Autistic children. PLoS ONE 2013, 8, e68322. [CrossRef] [PubMed]
26. Mosca, A.; Leclerc, M.; Hugot, J.P. Gut microbiota diversity and human diseases: Should we reintroduce key predators in our ecosystem? Front. Microbiol. 2016, 7, 455. [CrossRef] [PubMed]
27. Hold, G.L.; Smith, M.; Grange, C.; Watt, E.R.; El-Omar, E.M.; Mukhopadhya, I. Role of the gut microbiota in inflammatory bowel disease pathogenesis: What have we learnt in the past 10 years? World J. Gastroenterol. 2014, 20, 1192-1210. [CrossRef] [PubMed]
28. Keshavarzian, A.; Green, S.J.; Engen, P.A.; Voigt, R.M.; Naqib, A.; Forsyth, C.B.; Mutlu, E.; Shannon, K.M. Colonic bacterial composition in Parkinson's disease. Mov. Disord. 2015, 30, 1351-1360. [CrossRef] [PubMed]
29. Fernandes, J.; Su, W.; Rahat-Rozenbloom, S.; Wolever, T.M.; Comelli, E.M. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr. Diabetes 2014, 4, e121. [CrossRef] [PubMed]
30. Martínez, I.; Perdicaro, D.J.; Brown, A.W.; Hammons, S.; Carden, T.J.; Carr, T.P.; Eskridge, K.M.; Walter, J. Diet-induced alterations of host cholesterol metabolism are likely to affect the gut microbiota composition in hamsters. Appl. Environ. Microbiol. 2013, 79, 516-524. [CrossRef] [PubMed]
31. Voreades, N.; Kozil, A.; Weir, T.L. Diet and the development of the human intestinal microbiome. Front. Microbiol. 2014, 5, 494. [CrossRef] [PubMed]
32. Turroni, F.; Ribbera, A.; Foroni, E.; van Sinderen, D.; Ventura, M. Human gut microbiota and bifidobacteria: From composition to functionality. Antonie Van Leeuwenhoek 2008, 94, 35-50. [CrossRef] [PubMed]
33. Scott, K.P.; Gratz, S.W.; Sheridan, P.O.; Flint, H.J.; Duncan, S.H. The influence of diet on the gut microbiota. Pharmacol. Res. 2013, 69, 52-60. [CrossRef] [PubMed]
34. Arboleya, S.; Watkins, C.; Stanton, C.; Ross, R.P. Gut bifidobacteria populations in human health and aging. Front. Microbiol. 2016, 7, 1-9. [CrossRef] [PubMed]
35. Louis, P.; Young, P.; Holtrop, G.; Flint, H.J. Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ. Microbiol. 2010, 12, 304-314. [CrossRef] [PubMed]
36. Vital, M.; Howe, A.C.; Tiedje, J.M. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 2014, 5, e00889. [CrossRef] [PubMed]
37. Topping, D.L.; Clifton, P.M. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 2001, 81, 1031-1064. [PubMed]
38. Soret, R.; Chevalier, J.; De Coppet, P.; Poupeau, G.; Derkinderen, P.; Segain, J.P.; Neunlist, M. Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats. Gastroenterology 2010, 138. [CrossRef] [PubMed]
39. Canani, R.B.; Di Costanzo, M.; Leone, L.; Pedata, M.; Meli, R.; Calignano, A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 2011, 17, 1519-1528. [CrossRef] [PubMed]
40. Louis, P.; Hold, G.L.; Flint, H.J. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 2014, 12, 661-672. [CrossRef] [PubMed]
41. Salonen, A.; Lahti, L.; Salojarvi, J.; Holtrop, G.; Korpela, K.; Duncan, S.H.; Date, P.; Farquharson, F.; Johnstone, A.M.; Lobley, G.E et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014, 8, 2218-2230. [CrossRef] [PubMed]
42. El-Ansary, A.K.; Ben Bacha, A.; Kotb, M. Etiology of autistic features: The persisting neurotoxic effects of propionic acid. J. Neuroinflamm. 2012, 9, 74. [CrossRef] [PubMed]
43. Hughes, R.; Kurth, M.J.; McGilligan, V.; McGlynn, H.; Rowland, I. Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro. Nutr. Cancer 2008, 60, 259-266. [CrossRef] [PubMed]
44. De Angelis, M.; Piccolo, M.; Vannini, L.; Siragusa, S.; de Giacomo, A.; Serrazzanetti, D.I.; Cristofori, F.; Guerzoni, M.E.; Gobbetti, M.; Francavilla, R. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS ONE 2013, 8, e76993. [CrossRef] [PubMed]
45. Finegold, S.M. Desulfovibrio species are potentially important in regressive autism. Med. Hypotheses 2011, 77, 270-274. [CrossRef] [PubMed]
46. American Psychiatric Association. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders, 5th ed.; American Psychiatric Association: Arlington County, VA, USA, 2013.
47. Neul, J.L.; Kaufmann, W.E.; Glaze, D.G.; Christodoulou, J.; Clarke, A.J.; Bahi-Buisson, N.; Leonard, H.; Bailey, M.E.S.; Schanen, N.C.; Zappella, M et al. Rett syndrome: Revised diagnostic criteria and nomenclature. Ann. Neurol. 2010, 68, 944-950. [CrossRef] [PubMed]
48. Klaassen, C.D.; Cui, J.Y. Review: Mechanisms of how the intestinal microbiota alters the effects of drugs and bile acids. Drug Metab. Dispos. 2015, 43, 1505-1521. [CrossRef] [PubMed]
49. Lee, Y.K.; Menezes, J.S.; Umesaki, Y.; Mazmanian, S.K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 2011, 108, 4615-4622. [CrossRef] [PubMed]
50. Hsiao, E.Y.; McBride, S.W.; Hsien, S.; Sharon, G.; Hyde, E.R.; McCue, T.; Codelli, J.A.; Chow, J.; Reisman, S.E.; Petrosino, J.F et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013, 155, 1451-1463. [CrossRef] [PubMed]
51. De Theije, C.G.M.; Wopereis, H.; Ramadan, M.; van Eijndthoven, T.; Lambert, J.; Knol, J.; Garssen, J.; Kraneveld, A.D.; Oozeer, R. Altered gut microbiota and activity in a murine model of autism spectrum disorders. Brain. Behav. Immun. 2014, 37, 197-206. [CrossRef] [PubMed]
52. Nag, N.; Mellott, T.J.; Berger-Sweeney, J.E. Effects of postnatal dietary choline supplementation on motor regional brain volume and growth factor expression in a mouse model of Rett syndrome. Brain Res. 2008, 1237, 101-109. [CrossRef] [PubMed]
53. Park, M.J.; Aja, S.; Li, Q.; Degano, A.L.; Penati, J.; Zhuo, J.; Roe, C.R.; Ronnett, G.V. Anaplerotic triheptanoin diet enhances mitochondrial substrate use to remodel the metabolome and improve lifespan, motor function, and sociability in MeCP2-null mice. PLoS ONE 2014, 9, e109527. [CrossRef] [PubMed]
54. Neul, J.L.; Fang, P.; Barrish, J.; Lane, J.; Caeg, E.B.; Smith, E.O.; Zoghbi, H.; Percy, A.; Glaze, D.G. Specific mutations in methyl-CpG-binding protein 2 confer different severity in Rett syndrome. Neurology 2008, 70, 1313-1321. [CrossRef] [PubMed]
55. Klindworth, A.; Pruesse, E.; Schweer, T.; Peplies, J.; Quast, C.; Horn, M.; Glöckner, F.O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013, 41, e1. [CrossRef] [PubMed]
56. Weaver, G.A.; Tangel, C.T.; Krause, J.A.; Parfitt, M.M.; Jenkins, P.L.; Rader, J.M.; Lewis, B.A.; Miller, T.L.; Wolin, M.J. Acarbose enhances human colonic butyrate production. J. Nutr. 1997, 27, 717-723.
57. Masella, A.P.; Bartram, A.K.; Truszkowski, J.M.; Brown, D.G.; Neufeld, J.D. PANDAseq: Paired-end assembler for illumina sequences. BMC Bioinform. 2012, 13, 31. [CrossRef] [PubMed]
58. 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 2010, 7, 335-336. [CrossRef]
59. Edgar, R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26, 2460-2461. [CrossRef] [PubMed]
60. Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261-5267. [CrossRef] [PubMed]
61. Lozupone, C.; Knight, R. UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 2005, 71, 8228-8235. [CrossRef] [PubMed]
62. Langille, M.; Zaneveld, J.; Caporaso, J.G.; McDonald, D.; Knights, D.; Reyes, J.; Clemente, J.; Burkepile, D.; Vega Thurber, R.; Knight, R et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013, 31, 814-821. [CrossRef] [PubMed]
63. Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsky, L.; Garrett, W.S.; Huttenhower, C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12, R60. [CrossRef] [PubMed]