Cross-talk between the infant/maternal gut microbiota and the endocrine system: a promising topic of research

Francesca Turroni , Sonia Mirjam Rizzo , Marco Ventura , Sergio Bernasconi

Microbiome Research Reports ›› 2022, Vol. 1 ›› Issue (2) : 14

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Microbiome Research Reports ›› 2022, Vol. 1 ›› Issue (2) :14 DOI: 10.20517/mrr.2021.14
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Cross-talk between the infant/maternal gut microbiota and the endocrine system: a promising topic of research

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Abstract

The infant gut microbiota is the set of microorganisms colonizing the baby’s intestine. This complex ecosystem appears to be related to various physiological conditions of the host and it has also been shown to act as one of the most crucial determinants of infant’s health. Furthermore, the mother’s endocrine system, through its hormones, can have an effect on the composition of the newborn’s gut microbiota. In this perspective, we summarize the recent state of the art on the intricate relationships involving the intestinal microbiota and the endocrine system of mother/baby to underline the need to study the molecular mechanisms that appear to be involved.

Keywords

Infants / gut microbiota / endocrine system / thyroid / hormones

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Francesca Turroni, Sonia Mirjam Rizzo, Marco Ventura, Sergio Bernasconi. Cross-talk between the infant/maternal gut microbiota and the endocrine system: a promising topic of research. Microbiome Research Reports, 2022, 1(2): 14 DOI:10.20517/mrr.2021.14

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References

[1]

Hill CJ,Murphy K.Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET cohort.Microbiome2017;5:4 PMCID:PMC5240274

[2]

Korpela K,Moltu SJ.Intestinal microbiota development and gestational age in preterm neonates.Sci Rep2018;8:2453 PMCID:PMC5802739

[3]

Korpela K,Vepsäläinen O.Probiotic supplementation restores normal microbiota composition and function in antibiotic-treated and in caesarean-born infants.Microbiome2018;6:182 PMCID:PMC6192119

[4]

de Gunzburg J,Ducher A.Protection of the human gut microbiome from antibiotics.J Infect Dis2018;217:628-36 PMCID:PMC5853327

[5]

Mancabelli L,Lugli GA.Amoxicillin-clavulanic acid resistance in the genus.Bifidobacterium87:e03137-20 PMCID:PMC8091617

[6]

Browne HP,Forster SC.Transmission of the gut microbiota: spreading of health.Nat Rev Microbiol2017;15:531-43 PMCID:PMC5837012

[7]

Chu DM,Prince AL.Impact of maternal nutrition in pregnancy and lactation on offspring gut microbial composition and function.Gut Microbes2016;7:459-70 PMCID:PMC5103658

[8]

Cortes-Macías E,García-Mantrana I.Maternal diet shapes the breast milk microbiota composition and diversity: impact of mode of delivery and antibiotic exposure.J Nutr2021;151:330-40 PMCID:PMC7850106

[9]

Hjelmsø MH,Thorsen J.Prenatal dietary supplements influence the infant airway microbiota in a randomized factorial clinical trial.Nat Commun2020;11:426 PMCID:PMC6976654

[10]

Milani C,Bottacini F.The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota.Microbiol Mol Biol Rev2017;81:e00036-17 PMCID:PMC5706746

[11]

Stanislawski MA,Wagner BD.Gut microbiota in the first 2 years of life and the association with body mass index at age 12 in a norwegian birth cohort.mBio2018;9:e01751-18 PMCID:PMC6199494

[12]

Kimura I,Ohue-Kitano R.Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice.Science2020;367:eaaw8429

[13]

Saso A.Maternal immunization: nature meets nurture.Front Microbiol2020;11:1499 PMCID:PMC7396522

[14]

Hanson LA,Lundin S.The transfer of immunity from mother to child.Ann N Y Acad Sci2003;987:199-206

[15]

Rio-Aige K,Massot-Cladera M.Association of maternal microbiota and diet in cord blood cytokine and immunoglobulin profiles.Int J Mol Sci2021;22:1778 PMCID:PMC7916816

[16]

Sanidad KZ.Neonatal gut microbiome and immunity.Curr Opin Microbiol2020;56:30-7 PMCID:PMC8729197

[17]

Henrick BM,Lakshmikanth T.Bifidobacteria-mediated immune system imprinting early in life.Cell2021;184:3884-3898.e11

[18]

Adak A.An insight into gut microbiota and its functionalities.Cell Mol Life Sci2019;76:473-93

[19]

Clarke G,Scully P.The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner.Mol Psychiatry2013;18:666-73

[20]

Karakula-Juchnowicz H,Juchnowicz D.The study evaluating the effect of probiotic supplementation on the mental status, inflammation, and intestinal barrier in major depressive disorder patients using gluten-free or gluten-containing diet (SANGUT study): a 12-week, randomized, double-blind, and placebo-controlled clinical study protocol.Nutr J2019;18:50 PMCID:PMC6717641

[21]

Qi X,Pang Y.The impact of the gut microbiota on the reproductive and metabolic endocrine system.Gut Microbes2021;13:1-21 PMCID:PMC7971312

[22]

Hughes DT.Inter-kingdom signalling: communication between bacteria and their hosts.Nat Rev Microbiol2008;6:111-20 PMCID:PMC2667375

[23]

Boukerb AM,Rodrigues S.Inter-kingdom signaling of stress hormones: sensing, transport and modulation of bacterial physiology.Front Microbiol2021;12:690942 PMCID:PMC8526972

[24]

Lyte M.Catecholamine induced growth of gram negative bacteria.Life sci1992;50:203-12

[25]

Neuman H,Knight R.Microbial endocrinology: the interplay between the microbiota and the endocrine system.FEMS Microbiol Rev2015;39:509-21

[26]

Busnelli M,Chiesa G.The gut microbiota affects host pathophysiology as an endocrine organ: a focus on cardiovascular disease.Nutrients2019;12:79 PMCID:PMC7019666

[27]

Han H,Zhong R.From gut microbiota to host appetite: gut microbiota-derived metabolites as key regulators.Microbiome2021;9:162 PMCID:PMC8293578

[28]

Park S,Coupe B.The endoplasmic reticulum stress-autophagy pathway controls hypothalamic development and energy balance regulation in leptin-deficient neonates.Nat Commun2020;11:1914 PMCID:PMC7171135

[29]

Yao H,Fan X.Effects of gut microbiota on leptin expression and body weight are lessened by high-fat diet in mice.Br J Nutr2020;124:396-406

[30]

Song CH,Nam RH,Lee HN.17β-Estradiol supplementation changes gut microbiota diversity in intact and colorectal cancer-induced ICR male mice.Sci Rep2020;10:12283 PMCID:PMC7378548

[31]

Kaliannan K,Murphy K.Estrogen-mediated gut microbiome alterations influence sexual dimorphism in metabolic syndrome in mice.Microbiome2018;6:205 PMCID:PMC6234624

[32]

Harada N,Hanada K.Relationship between gut environment, feces-to-food ratio, and androgen deficiency-induced metabolic disorders.Gut Microbes2020;12:1817719 PMCID:PMC7781658

[33]

Colldén H,Wallenius V.The gut microbiota is a major regulator of androgen metabolism in intestinal contents.Am J Physiol Endocrinol Metab2019;317:E1182-92 PMCID:PMC6962501

[34]

Caricilli AM.The role of gut microbiota on insulin resistance.Nutrients2013;5:829-51 PMCID:PMC3705322

[35]

Lee CJ,Maruthur N.Gut microbiome and its role in obesity and insulin resistance.Ann N Y Acad Sci2020;1461:37-52

[36]

Han Q,Li W,Du Y.Androgen-induced gut dysbiosis disrupts glucolipid metabolism and endocrinal functions in polycystic ovary syndrome.Microbiome2021;9:101 PMCID:PMC8103748

[37]

Barroso A,Perdices-Lopez C.Neonatal exposure to androgens dynamically alters gut microbiota architecture.J Endocrinol2020;247:69-85

[38]

Tett A,Masetti G,Segata N.Prevotella diversity, niches and interactions with the human host.Nat Rev Microbiol2021;19:585-99

[39]

Yang H,Li S.Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity.NPJ Biofilms Microbiomes2020;6:32 PMCID:PMC7486914

[40]

DiGiulio DB,McMurdie PJ.Temporal and spatial variation of the human microbiota during pregnancy.Proc Natl Acad Sci U S A2015;112:11060-5 PMCID:PMC4568272

[41]

Mallott EK,Koenig A,Lu A.Reproductive hormones mediate changes in the gut microbiome during pregnancy and lactation in Phayre's leaf monkeys.Sci Rep2020;10:9961 PMCID:PMC7305161

[42]

Nuriel-Ohayon M,Ziv O.Progesterone increases bifidobacterium relative abundance during late pregnancy.Cell Rep2019;27:730-736.e3

[43]

Doden HL,Mythen SM.Structural and biochemical characterization of 20β-hydroxysteroid dehydrogenase from.Bifidobacterium adolescentis294:12040-53 PMCID:PMC6690682

[44]

Dahl C,Iszatt N.Gut microbiome of mothers delivering prematurely shows reduced diversity and lower relative abundance of bifidobacterium and streptococcus.PLoS One2017;12:e0184336 PMCID:PMC5656300

[45]

Duranti S,Lugli GA.Insights from genomes of representatives of the human gut commensal bifidobacterium bifidum.Environ Microbiol2015;17:2515-31

[46]

Duranti S,Mancabelli L.Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission.Microbiome2017;5:66 PMCID:PMC5485682

[47]

Markle JG,Mortin-Toth S.Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity.Science2013;339:1084-8

[48]

Li S.Role of biological sex in the cardiovascular-gut microbiome axis.Front Cardiovasc Med2021;8:759735 PMCID:PMC8785253

[49]

Org E,Parks BW.Sex differences and hormonal effects on gut microbiota composition in mice.Gut Microbes2016;7:313-22 PMCID:PMC4988450

[50]

Liu P,Zhang N,Luo B.Crosstalk between the gut microbiota and the brain: an update on neuroimaging findings.Front Neurol2019;10:883 PMCID:PMC6700295

[51]

Sherman MP,Niklas V.Gut microbiota, the immune system, and diet influence the neonatal gut-brain axis.Pediatr Res2015;77:127-35

[52]

Keskitalo A,Kortesluoma S.Gut microbiota diversity but not composition is related to saliva cortisol stress response at the age of 2.5 months.Stress2021;24:551-60

[53]

Yang I,Brennan PA,Murphy JR.The infant microbiome: implications for infant health and neurocognitive development.Nurs Res2016;65:76-88 PMCID:PMC4681407

[54]

Misiak B,Marlicz W.The HPA axis dysregulation in severe mental illness: can we shift the blame to gut microbiota?.Prog Neuropsychopharmacol Biol Psychiatry2020;102:109951

[55]

Tsigos C.Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress.J Psychosom Res2002;53:865-71

[56]

Kelly JR,Cryan JF,Dinan TG.Mood and microbes: gut to brain communication in depression.Gastroenterol Clin North Am2019;48:389-405

[57]

Kelly JR,O' Brien C.Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat.J Psychiatr Res2016;82:109-18

[58]

Rosin S,Azcarate-Peril MA.A preliminary study of gut microbiome variation and HPA axis reactivity in healthy infants.Psychoneuroendocrinology2021;124:105046 PMCID:PMC8121098

[59]

Zijlmans MA,Riksen-Walraven JM,de Weerth C.Maternal prenatal stress is associated with the infant intestinal microbiota.Psychoneuroendocrinology2015;53:233-45

[60]

Rodriguez N,Field CJ,Scott JA.Prenatal Depression, Breastfeeding, and Infant Gut Microbiota.Front Microbiol2021;12:664257 PMCID:PMC8363245

[61]

Jahnke JR,Azcarate-Peril MA.Maternal precarity and HPA axis functioning shape infant gut microbiota and HPA axis development in humans.PLoS One2021;16:e0251782 PMCID:PMC8136730

[62]

Weerth C. Do bacteria shape our development?.Neurosci Biobehav Rev2017;83:458-71

[63]

Theiler-Schwetz V,Schlager H,Fickert P.Bile acids and glucocorticoid metabolism in health and disease.Biochim Biophys Acta Mol Basis Dis2019;1865:243-51

[64]

Kelly JR,Cryan JF,Clarke G.Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders.Front Cell Neurosci2015;9:392 PMCID:PMC4604320

[65]

Bloemendaal M,Belzer C.Probiotics-induced changes in gut microbial composition and its effects on cognitive performance after stress: exploratory analyses.Transl Psychiatry2021;11:300 PMCID:PMC8137885

[66]

Korpela K,Kolho KL.Maternal fecal microbiota transplantation in cesarean-born infants rapidly restores normal gut microbial development: a proof-of-concept study.Cell2020;183:324-334.e5

[67]

Sarkar A,Harty S,Cryan JF.Psychobiotics and the manipulation of bacteria-gut-brain signals.Trends Neurosci2016;39:763-81 PMCID:PMC5102282

[68]

Cheng LH,Wu CC,Tsai YC.Psychobiotics in mental health, neurodegenerative and neurodevelopmental disorders.J Food Drug Anal2019;27:632-48

[69]

Badillo-Suárez PA,Nieves-Morales X.Impact of metabolic hormones secreted in human breast milk on nutritional programming in childhood obesity.J Mammary Gland Biol Neoplasia2017;22:171-91

[70]

Wan Y,Lu M.Human milk microbiota development during lactation and its relation to maternal geographic location and gestational hypertensive status.Gut Microbes2020;11:1438-49 PMCID:PMC7524296

[71]

Bravi F,Decarli A,Agostoni C.Impact of maternal nutrition on breast-milk composition: a systematic review.Am J Clin Nutr2016;104:646-62

[72]

Andreas NJ,Mehring Le-Doare K.Human breast milk: a review on its composition and bioactivity.Early Hum Dev2015;91:629-35

[73]

Victora CG,Barros AJ,Horton S.Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect.Lancet2016;387:475-90

[74]

Lind MV,Mølgaard C.Breastfeeding, breast milk composition, and growth outcomes. In: Colombo J, Koletzko B, Lampl M, editors. Recent Research in Nutrition and Growth. S. Karger AG; 2018. p. 63-77.

[75]

Cabrera-Rubio R,Laitinen K,Isolauri E.The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery.Am J Clin Nutr2012;96:544-51

[76]

Collado MC,Salminen S.Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk.Pediatr Res2012;72:77-85

[77]

Gomez-Gallego C,Salminen S.The human milk microbiome and factors influencing its composition and activity.Semin Fetal Neonatal Med2016;21:400-5

[78]

Anderson G,Maes M.Breastfeeding and the gut-brain axis: is there a role for melatonin?.Biomol Concepts2017;8:185-95

[79]

Xia S,Li Y.Effects of melatonin on intestinal function and bacterial compositions in sucking piglets.J Anim Physiol Anim Nutr (Berl)2022;

[80]

Paulose JK.The melatonin-sensitive circadian clock of the enteric bacterium Enterobacter aerogenes.Gut Microbes2016;7:424-7 PMCID:PMC5154366

[81]

Sinha RA,Yen PM.Direct effects of thyroid hormones on hepatic lipid metabolism.Nat Rev Endocrinol2018;14:259-69 PMCID:PMC6013028

[82]

Cuan-Baltazar Y.Microorganisms associated to thyroid autoimmunity.Autoimmun Rev2020;19:102614

[83]

Zhang D,Wang G.Trimester-specific reference ranges for thyroid hormones in pregnant women.Medicine (Baltimore)2019;98:e14245 PMCID:PMC6358369

[84]

Virili C.Does microbiota composition affect thyroid homeostasis?.Endocrine2015;49:583-7

[85]

Su X,Li Y,Wang Z.Gut dysbiosis is associated with primary hypothyroidism with interaction on gut-thyroid axis.Clin Sci (Lond)2020;134:1521-35

[86]

Knezevic J,Tmava Berisha A.Thyroid-gut-axis: how does the microbiota influence thyroid function?.Nutrients2020;12:1769 PMCID:PMC7353203

[87]

Bargiel P,Stachowska L.Microbiome metabolites and thyroid dysfunction.J Clin Med2021;10:3609 PMCID:PMC8397005

[88]

Zhao F,Li J.Alterations of the gut microbiota in hashimoto’s thyroiditis patients.Thyroid2018;28:175-86

[89]

Magne F,Gauthier L.The firmicutes/bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients?.Nutrients2020;12:1474 PMCID:PMC7285218

[90]

Koppel N,Balskus EP.Chemical transformation of xenobiotics by the human gut microbiota.Science2017;356:eaag2770 PMCID:PMC5534341

[91]

Yao Z,Gong Y.Relation of gut microbes and L-Thyroxine through altered thyroxine metabolism in subclinical hypothyroidism subjects.Front Cell Infect Microbiol2020;10:495 PMCID:PMC7531258

[92]

Sun J,Lin B.Gut microbiota participates in antithyroid drug induced liver injury through the lipopolysaccharide related signaling pathway.Front Pharmacol2020;11:598170 PMCID:PMC7774100

[93]

Hazenberg MP,Visser TJ.Hydrolysis of iodothyronine conjugates by intestinal bacteria.FEMS Microbiol Rev1988;4:9-16

[94]

Dabek M,Stevens VJ,Louis P.Distribution of beta-glucosidase and beta-glucuronidase activity and of beta-glucuronidase gene gus in human colonic bacteria.FEMS Microbiol Ecol2008;66:487-95

[95]

Dashnyam P,Hsieh TJ.β-Glucuronidases of opportunistic bacteria are the major contributors to xenobiotic-induced toxicity in the gut.Sci Rep2018;8:16372 PMCID:PMC6219552

[96]

Jones BV,Hill C,Marchesi JR.Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome.Proc Natl Acad Sci U S A2008;105:13580-5 PMCID:PMC2533232

[97]

Virili C.“With a little help from my friends” - The role of microbiota in thyroid hormone metabolism and enterohepatic recycling.Mol Cell Endocrinol2017;458:39-43

[98]

Virili C,Centanni M.Gut microbiome and thyroid autoimmunity.Best Pract Res Clin Endocrinol Metab2021;35:101506

[99]

Feng J,Sun J.Alterations in the gut microbiota and metabolite profiles of thyroid carcinoma patients.Int J Cancer2019;144:2728-45

[100]

Zhang J,Zhao C.Dysbiosis of the gut microbiome is associated with thyroid cancer and thyroid nodules and correlated with clinical index of thyroid function.Endocrine2019;64:564-74

[101]

Li A,Gao X.Gut microbiome alterations in patients with thyroid nodules.Front Cell Infect Microbiol2021;11:643968 PMCID:PMC8005713

[102]

Aranda A.MicroRNAs and thyroid hormone action.Mol Cell Endocrinol2021;525:111175

[103]

Taniguchi K,Akao Y.PTBP1-targeting microRNAs regulate cancer-specific energy metabolism through the modulation of PKM1/M2 splicing.Cancer Sci2021;112:41-50 PMCID:PMC7780020

[104]

Kon IY,Gmoshinskaya MV.The study of breast milk IGF-1, leptin, ghrelin and adiponectin levels as possible reasons of high weight gain in breast-fed infants.Ann Nutr Metab2014;65:317-23

[105]

Perry B.Appetite regulation and weight control: the role of gut hormones.Nutr Diabetes2012;2:e26 PMCID:PMC3302146

[106]

Whitmore TJ,Graham DF.Analysis of insulin in human breast milk in mothers with type 1 and type 2 diabetes mellitus.Int J Endocrinol2012;2012:296368 PMCID:PMC3303574

[107]

Granata R,Luque RM.Obestatin regulates adipocyte function and protects against diet-induced insulin resistance and inflammation.FASEB J2012;26:3393-411

[108]

Ilcol YO,Eroz E.Resistin is present in human breast milk and it correlates with maternal hormonal status and serum level of C-reactive protein.Clin Chem Lab Med2008;46:118-24

[109]

Kelly DP.Medicine. Irisin, light my fire.Science2012;336:42-3

[110]

Aydin S,Aydin S.Copeptin, adropin and irisin concentrations in breast milk and plasma of healthy women and those with gestational diabetes mellitus.Peptides2013;47:66-70

[111]

Castan-Laurell I,Daviaud D.Effect of hypocaloric diet-induced weight loss in obese women on plasma apelin and adipose tissue expression of apelin and APJ.Eur J Endocrinol2008;158:905-10 PMCID:PMC2683032

[112]

Dong J,Jiang ZY.Nesfatin-1 influences the excitability of glucosensing neurons in the dorsal vagal complex and inhibits food intake.PLoS One2014;9:e98967 PMCID:PMC4048226

[113]

Schueler J,Hart AM,Larson-Meyer DE.Presence and dynamics of leptin, GLP-1, and PYY in human breast milk at early postpartum.Obesity (Silver Spring)2013;21:1451-8 PMCID:PMC3742570

[114]

Elmlinger MW,Loui A,Obladen M.Insulin-like growth factors and binding proteins in early milk from mothers of preterm and term infants.Horm Res2007;68:124-31

[115]

Entringer S.Impact of stress and stress physiology during pregnancy on child metabolic function and obesity risk.Curr Opin Clin Nutr Metab Care2013;16:320-7 PMCID:PMC3740218

[116]

Esposito S,D'Alonzo R.Pediatric sleep disturbances and treatment with melatonin.J Transl Med2019;17:77 PMCID:PMC6419450

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