Glycated milk protein fermented with Lactobacillus rhamnosus ameliorates the cognitive health of mice under mild-stress condition

References

• Li S, Wang C, Wang W, Dong H, Hou P, Tang Y. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci. 2008;82(17–18):934–942. doi:10.1016/j.lfs.2008.02.010.
   Google Scholar
• Foster JA, Rinaman L, Cryan JF. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol Stress. 2017;7:124–136. doi:10.1016/j.ynstr.2017.03.001.
   Google Scholar
• Mayer EA, Savidge T, Shulman RJ. Brain-gut microbiome interactions and functional bowel disorders. Gastroenterology. 2014;146(6):1500–1512. doi:10.1053/j.gastro.2014.02.037.
   Google Scholar
• Matsui F, Morimoto M, Yoshimoto K, Nakatomi Y, Syoji H, Nishimura A, Isoda K, Tanda K, Hosoi H. Effects of stress of postnatal development on corticosterone, serotonin and behavioral changes. Brain Dev. 2010;32(7):517–523. doi:10.1016/j.braindev.2009.09.001.
   Google Scholar
• Kyrou I, Tsigos C. Stress mechanisms and metabolic complications. Horm Metab Res. 2007;39(6):430–438. doi:10.1055/s-2007-981462.
   Google Scholar
• Urita Y, Goto M, Watanabe T, Matsuzaki M, Gomi A, Kano M. Continuous consumption of fermented milk containing Bifidobacterium bifidum YIT 10347 improves gastrointestinal and psychological symptoms in patients with functional gastrointestinal disorders. Biosci Microbiota Food Health. 2015;34(2):37–44. doi:10.12938/bmfh.2014-017.
   Google Scholar
• Dela Pena IJ, Hong E, de la Pena JB, Kim HJ, Botanas CJ, Hong YS, Hwang YS, Moon BS, Cheong JH. Milk collected at night induces sedative and anxiolytic-like effects and augments pentobarbital-induced sleeping behavior in mice. J Med Food. 2015;18(11):1255–1261. doi:10.1089/jmf.2015.3448.
   Google Scholar
• Markus CR, Olivier B, de Haan EH. Whey protein rich in alpha-lactalbumin increases the ratio of plasma tryptophan to the sum of the other large neutral amino acids and improves cognitive performance in stress-vulnerable subjects. Am J Clin Nutr. 2002;75(6):1051–1056. doi:10.1093/ajcn/75.6.1051.
   Google Scholar
• Messaoudi M, Lefranc-Millot C, Desor D, Demagny B, Bourdon L. Effects of a tryptic hydrolysate from bovine milk alphaS1-casein on hemodynamic responses in healthy human volunteers facing successive mental and physical stress situations. Eur J Nutr. 2005;44(2):128–132. doi:10.1007/s00394-004-0534-7.
   Google Scholar
• Oh NS, Joung JY, Lee JY, Kim Y, Kim SH. Enhancement of antioxidative and intestinal anti-inflammatory activities of glycated milk casein after fermentation with Lactobacillus rhamnosus 4B15. J Agric Food Chem. 2017;65(23):4744–4754. doi:10.1021/acs.jafc.7b01339.
   Google Scholar
• Oh NS, Joung JY, Lee JY, Kim Y. Probiotic and anti-inflammatory potential of Lactobacillus rhamnosus 4B15 and Lactobacillus gasseri 4M13 isolated from infant feces. PLoS One. 2018;13(2):e0192021. doi:10.1371/journal.pone.0192021.
   Google Scholar
• Meziane H, Ouagazzal AM, Aubert L, Wietrzych M, Krezel W. Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav. 2007;6(2):192–200. doi:10.1111/j.1601-183X.2006.00249.x.
   Google Scholar
• Ter Horst JP, de Kloet ER, Schachinger H, Oitzl MS. Relevance of stress and female sex hormones for emotion and cognition. Cell Mol Neurobiol. 2012;32(5):725–735. doi:10.1007/s10571-011-9774-2.
   Google Scholar
• Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002;32(6):435–443. doi:10.1023/A:1020884312053.
   Google Scholar
• Li W, Zhou SP, Jin YP, Huang XF, Zhou W, Han M, Yu Y, Yan K-J, Li S-M, Ma X-H, et al. Salvianolic acids T and U: a pair of atropisomeric trimeric caffeic acids derivatives from root of Salvia miltiorrhiza. Fitoterapia. 2014;98:248–253. doi:10.1016/j.fitote.2014.08.018.
   Google Scholar
• Katz RJ. Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacol Biochem Behav. 1982;16(6):965–968. doi:10.1016/0091-3057(82)90053-3.
   Google Scholar
• Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007;2(2):322–328. doi:10.1038/nprot.2007.44.
   Google Scholar
• Oh NS, Park MR, Lee KW, Kim SH, Kim Y. Dietary Maillard reaction products and their fermented products reduce cardiovascular risk in an animal model. J Dairy Sci. 2015;98(8):5102–5112. doi:10.3168/jds.2015-9308.
   Google Scholar
• Kim BK, Lee IO, Tan PL, Eor JY, Hwang JK, Kim SH. Protective effect of Lactobacillus fermentum LA12 in an alcohol-induced rat model of alcoholic steatohepatitis. Korean J Food Sci An. 2017;37:931–939.
   Google Scholar
• Mateer SW, Cardona J, Marks E, Goggin BJ, Hua S, Keely S. Ex vivo intestinal sacs to assess mucosal permeability in models of gastrointestinal disease. J Vis Exp. 2016;(108):e53250.
   Google Scholar
• Renju GL, Muraleedhara Kurup G, Bandugula VR. Effect of lycopene isolated from Chlorella marina on proliferation and apoptosis in human prostate cancer cell line PC-3. Tumour Biol. 2014;35(11):10747–10758. doi:10.1007/s13277-014-2339-5.
   Google Scholar
• Natarajan R, Forrester L, Chiaia NL, Yamamoto BK. Chronic-stress-induced behavioral changes associated with subregion-selective serotonin cell death in the dorsal raphe. J Neurosci. 2017;37(26):6214–6223. doi:10.1523/JNEUROSCI.3781-16.2017.
   Google Scholar
• Grimm S, Wirth K, Fan Y, Weigand A, Gartner M, Feeser M, Dziobek I, Bajbouj M, Aust S. The interaction of corticotropin-releasing hormone receptor gene and early life stress on emotional empathy. Behav Brain Res. 2017;329:180–185. doi:10.1016/j.bbr.2017.04.047.
   Google Scholar
• Evanson NK, Herman JP. Metabotropic glutamate receptor-mediated signaling dampens the HPA axis response to restraint stress. Physiol Behav. 2015;150:2–7. doi:10.1016/j.physbeh.2015.02.027.
   Google Scholar
• Ulven T. Short-chain free fatty acid receptors FFA2/GPR43 and FFA3/GPR41 as new potential therapeutic targets. Front Endocrinol (Lausanne). 2012;3:111. doi:10.3389/fendo.2012.00111.
   Google Scholar
• DM F, Bossy-Wetzel E, NJ W, TG C, DR G. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem. 1999;274(4):2225–2233. doi:10.1074/jbc.274.4.2225.
   Google Scholar
• Jin Y, Fan JT, Gu XL, Zhang LY, Han J, Du SH, et al. Neuroprotective activity of cerebrosides from Typhonium giganteum by regulating Caspase-3 and Bax/Bcl-2 signaling pathways in PC12 cells. J Nat Prod. 2017;80(6):1734–1741. doi:10.1021/acs.jnatprod.6b00954.
   Google Scholar
• Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57(2):173–185. doi:10.1124/pr.57.2.4.
   Google Scholar
• McGaughey KD, Yilmaz-Swenson T, Elsayed NM, Cruz DA, Rodriguiz RM, Kritzer MD, Peterchev AV, Roach J, Wetsel WC, Williamson DE, et al. Relative abundance of Akkermansia spp. and other bacterial phylotypes correlates with anxiety- and depressive-like behavior following social defeat in mice. Sci Rep. 2019;9(1):3281. doi:10.1038/s41598-019-40140-5.
   Google Scholar
• Prehn-Kristensen A, Zimmermann A, Tittmann L, Lieb W, Schreiber S, Baving L, Fischer A. Reduced microbiome alpha diversity in young patients with ADHD. PLoS One. 2018;13(7):e0200728. doi:10.1371/journal.pone.0200728.
   Google Scholar
• Karl JP, Hatch AM, Arcidiacono SM, Pearce SC, Pantoja-Feliciano IG, Doherty LA, et al. Effects of psychological, environmental and physical stressors on the gut microbiota. Front Microbiol. 2018;9:2013.
   Google Scholar
• Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: A Common Factor in Human Diseases. Biomed Res Int. 2017;2017:9351507. doi:10.1155/2017/9351507.
   Google Scholar
• McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007;87(3):873–904. doi:10.1152/physrev.00041.2006.
   Google Scholar
• Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol. 2006;572(1):31–44. doi:10.1113/jphysiol.2006.105254.
   Google Scholar
• Zareie M, Johnson-Henry K, Jury J, Yang PC, Ngan BY, McKay DM, Soderholm JD, Perdue MH, Sherman PM. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut. 2006;55(11):1553–1560. doi:10.1136/gut.2005.080739.
   Google Scholar
• Kaster MP, Machado NJ, Silva HB, Nunes A, Ardais AP, Santana M, Baqi Y, Müller CE, Rodrigues ALS, Porciúncula LO, et al. Caffeine acts through neuronal adenosine A 2A receptors to prevent mood and memory dysfunction triggered by chronic stress. Proc Natl Acad Sci U S A. 2015;112(25):7833–7838. doi:10.1073/pnas.1423088112.
   Google Scholar
• Mohammadi HS, Goudarzi I, Lashkarbolouki T, Abrari K, Elahdadi Salmani M. Chronic administration of quercetin prevent spatial learning and memory deficits provoked by chronic stress in rats. Behav Brain Res. 2014;270:196–205. doi:10.1016/j.bbr.2014.05.015.
   Google Scholar
• Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, Dinan TG, Cryan JF. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry. 2013;18(6):666–673. doi:10.1038/mp.2012.77.
   Google Scholar
• Foster JA, McVey Neufeld KA. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305–312. doi:10.1016/j.tins.2013.01.005.
   Google Scholar
• Xu RJ. Bioactive peptides in milk and their biological and health implications. Food Rev Int. 1998;14(1):1–16. doi:10.1080/87559129809541147.
   Google Scholar
• Li S, Wang Z, Yang Y, Yang S, Yao C, Liu K, Cui S, Zou Q, Sun H, Guo G, et al. Lachnospiraceae shift in the microbial community of mice faecal sample effects on water immersion restraint stress. AMB Express. 2017;7(1):82. doi:10.1186/s13568-017-0383-4.
   Google Scholar
• Burokas A, Arboleya S, Moloney RD, Peterson VL, Murphy K, Clarke G, Stanton C, Dinan TG, Cryan JF. Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry. 2017;82(7):472–487. doi:10.1016/j.biopsych.2016.12.031.
   Google Scholar
• Arboleya S, Sanchez B, Milani C, Duranti S, Solis G, Fernandez N, de Los Reyes-gavilán CG, Ventura M, Margolles A, Gueimonde M, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015;166(3):538–544. doi:10.1016/j.jpeds.2014.09.041.
   Google Scholar
• Potter E, Sutton S, Donaldson C, Chen R, Perrin M, Lewis K, Sawchenko PE, Vale W. Distribution of corticotropin-releasing factor receptor mRNA expression in the rat brain and pituitary. Proc Natl Acad Sci U S A. 1994;91(19):8777–8781. doi:10.1073/pnas.91.19.8777.
   Google Scholar
• Bale TL, Vale WW. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol. 2004;44(1):525–557. doi:10.1146/annurev.pharmtox.44.101802.121410.
   Google Scholar
• Yuste R, Katz LC. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron. 1991;6(3):333–344. doi:10.1016/0896-6273(91)90243-S.
   Google Scholar
• Kim JJ, Yoon KS. Stress: metaplastic effects in the hippocampus. Trends Neurosci. 1998;21(12):505–509. doi:10.1016/S0166-2236(98)01322-8.
   Google Scholar
• Banasr M, Hery M, Printemps R, Daszuta A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology. 2004;29(3):450–460. doi:10.1038/sj.npp.1300320.
   Google Scholar
• Hosang GM, Shiles C, Tansey KE, McGuffin P, Uher R. Interaction between stress and the BDNF Val66Met polymorphism in depression: a systematic review and meta-analysis. BMC Med. 2014;12:7. doi:10.1186/1741-7015-12-7.
   Google Scholar
• Aydemir C, Yalcin ES, Aksaray S, Kisa C, Yildirim SG, Uzbay T, et al. Brain-derived neurotrophic factor (BDNF) changes in the serum of depressed women. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30(7):1256–1260. doi:10.1016/j.pnpbp.2006.03.025.
   Google Scholar
• Jacobsen JP, Mork A. Chronic corticosterone decreases brain-derived neurotrophic factor (BDNF) mRNA and protein in the hippocampus, but not in the frontal cortex, of the rat. Brain Res. 2006;1110(1):221–225. doi:10.1016/j.brainres.2006.06.077.
   Google Scholar
• Marin IA, Goertz JE, Ren T, Rich SS, Onengut-Gumuscu S, Farber E, Wu M, Overall CC, Kipnis J, Gaultier A, et al. Microbiota alteration is associated with the development of stress-induced despair behavior. Sci Rep. 2017:43859. doi:10.1038/srep43859.
   Google Scholar
• Wong ML, Inserra A, Lewis MD, Mastronardi CA, Leong L, Choo J. Inflammasome signaling affects anxiety- and depressive-like behavior and gut microbiome composition. Mol Psychiatry. 2016;21(6):797–805. doi:10.1038/mp.2016.46.
   Google Scholar
• Garcia-Bueno B, Caso JR, Leza JC. Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev. 2008;32(6):1136–1151. doi:10.1016/j.neubiorev.2008.04.001.
   Google Scholar
• Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol. 2006;147(Suppl 1):S232–40. doi:10.1038/sj.bjp.0706400.
   Google Scholar
• Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron. 2008;57(2):178–201. doi:10.1016/j.neuron.2008.01.003.
   Google Scholar
• Brzozowski B, Mazur-Bialy A, Pajdo R, Kwiecien S, Bilski J, Zwolinska-Wcislo M, Mach T, Brzozowski T. Mechanisms by which stress affects the experimental and clinical inflammatory bowel disease (IBD): role of brain-gut axis. Curr Neuropharmacol. 2016;14(8):892–900. doi:10.2174/1570159X14666160404124127.
   Google Scholar
• Kelly JR, Kennedy PJ, Cryan JF, Dinan TG, Clarke G, Hyland NP. Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci. 2015;9:392. doi:10.3389/fncel.2015.00392.
   Google Scholar
• Bercik P, Denou E, Collins J, Jackson W, Lu J, Jury J, Deng Y, Blennerhassett P, Macri J, McCoy KD, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011;141(2):599–609.e1–3. doi:10.1053/j.gastro.2011.04.052.
   Google Scholar
• Wang H, Lee IS, Braun C, Enck P. Effect of probiotics on central nervous system functions in animals and humans: a systematic review. J Neurogastroenterol Motil. 2016;22(4):589–605. doi:10.5056/jnm16018.
   Google Scholar
• Yun B, Yoo JY, Park MR, Ryu S, Lee WJ, Choi HJ, Kang MK, Kim Y, Oh S. Ingestion of Gouda cheese ameliorates the chronic unpredictable mild stress in mice. Food Sci Anim Resour. 2020;40(1):145–153. doi:10.5851/kosfa.2019.e81.
   Google Scholar