Long-Term Implicit Epigenetic Stress Information in the Enteric Nervous System and its Contribution to Developing and Perpetuating IBS


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Abstract

:Psychiatric and mood disorders may play an important role in the development and persistence of irritable bowel syndrome (IBS). Previously, we hypothesized that stress-induced implicit memories may persist throughout life via epigenetic processes in the enteric nervous system (ENS), independent of the central nervous system (CNS). These epigenetic memories in the ENS may contribute to developing and perpetuating IBS. Here, we further elaborate on our earlier hypothesis. That is, during pregnancy, maternal prenatal stresses perturb the HPA axis and increase circulating cortisol levels, which can affect the maternal gut microbiota. Maternal cortisol can cross the placental barrier and increase cortisol-circulating levels in the fetus. This leads to dysregulation of the HPA axis, affecting the gut microbiota, microbial metabolites, and intestinal permeability in the fetus. Microbial metabolites, such as short-chain fatty acids (which also regulate the development of fetal ENS), can modulate a range of diseases by inducing epigenetic changes. These mentioned processes suggest that stress-related, implicit, long-term epigenetic memories may be programmed into the fetal ENS during pregnancy. Subsequently, this implicit epigenetic stress information from the fetal ENS could be conveyed to the CNS through the bidirectional microbiota-gut-brain axis (MGBA), leading to perturbed functional connectivity among various brain networks and the dysregulation of affective and pain processes.

About the authors

Császár-Nagy Noemi

, National University of Public Services

Email: info@benthamscience.net

Petr Bob

Center for Neuropsychiatric Research of Traumatic Stress, Department of Psychiatry & UHSL, First Faculty of Medicine, and Department of Psychiatry, Faculty of Medicine Pilsen, Charles University

Email: info@benthamscience.net

István Bókkon

, Psychosomatic Outpatient Clinics

Author for correspondence.
Email: info@benthamscience.net

References

  1. Chen, J.; Barandouzi, Z.A.; Lee, J.; Xu, W.; Feng, B.; Starkweather, A.; Cong, X. Psychosocial and sensory factors contribute to self-reported pain and quality of life in young adults with irritable bowel syndrome. Pain Manag. Nurs., 2022, 23(5), 646-654. doi: 10.1016/j.pmn.2021.12.004 PMID: 35074280
  2. Tripathi, R.; Mehrotra, S. Irritable bowel syndrome and its psychological management. Ind. Psychiatry J., 2015, 24(1), 91-93. doi: 10.4103/0972-6748.160947 PMID: 26257492
  3. van Tilburg, M.A.L.; Palsson, O.S.; Whitehead, W.E. Which psychological factors exacerbate irritable bowel syndrome? Development of a comprehensive model. J. Psychosom. Res., 2013, 74(6), 486-492. doi: 10.1016/j.jpsychores.2013.03.004 PMID: 23731745
  4. Sharkey, K.A.; Mawe, G.M. The enteric nervous system. Physiol. Rev., 2023, 103(2), 1487-1564. doi: 10.1152/physrev.00018.2022 PMID: 36521049
  5. Furness, J.B. Comparative and evolutionary aspects of the digestive system and its enteric nervous system control. Adv. Exp. Med. Biol., 2022, 1383, 165-177. doi: 10.1007/978-3-031-05843-1_16 PMID: 36587156
  6. Green, S.A.; Uy, B.R.; Bronner, M.E. Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest. Nature, 2017, 544(7648), 88-91. doi: 10.1038/nature21679 PMID: 28321127
  7. Furness, J.B.; Stebbing, M.J. The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems. Neurogastroenterol. Motil., 2018, 30(2), e13234. doi: 10.1111/nmo.13234 PMID: 29024273
  8. Császár-Nagy, N.; Bókkon, I. Hypnotherapy and IBS: Implicit, long-term stress memory in the ENS? Heliyon, 2023, 9(1), e12751. doi: 10.1016/j.heliyon.2022.e12751 PMID: 36685398
  9. Mao, C.P.; Chen, F.R.; Huo, J.H.; Zhang, L.; Zhang, G.R.; Zhang, B.; Zhou, X.Q. Altered resting‐state functional connectivity and effective connectivity of the habenula in irritable bowel syndrome: A cross‐sectional and machine learning study. Hum. Brain Mapp., 2020, 41(13), 3655-3666. doi: 10.1002/hbm.25038 PMID: 32488929
  10. Weng, Y.; Qi, R.; Liu, C.; Ke, J.; Xu, Q.; Wang, F.; Zhang, L.J.; Lu, G.M. Disrupted functional connectivity density in irritable bowel syndrome patients. Brain Imaging Behav., 2017, 11(6), 1812-1822. doi: 10.1007/s11682-016-9653-z PMID: 27848148
  11. Bhatt, R.R.; Gupta, A.; Labus, J.S.; Zeltzer, L.K.; Tsao, J.C.; Shulman, R.J.; Tillisch, K. Altered brain structure and functional connectivity and its relation to pain perception in girls with irritable bowel syndrome. Psychosom. Med., 2019, 81(2), 146-154. doi: 10.1097/PSY.0000000000000655 PMID: 30615602
  12. Nisticò, V.; Rossi, R.E.; D’Arrigo, A.M.; Priori, A.; Gambini, O.; Demartini, B. Functional neuroimaging in irritable bowel syndrome: A systematic review highlights common brain alterations with functional movement disorders. J. Neurogastroenterol. Motil., 2022, 28(2), 185-203. doi: 10.5056/jnm21079 PMID: 35189600
  13. Qi, R.; Liu, C.; Weng, Y.; Xu, Q.; Chen, L.; Wang, F.; Zhang, L.J.; Lu, G.M. Disturbed interhemispheric functional connectivity rather than structural connectivity in irritable bowel syndrome. Front. Mol. Neurosci., 2016, 9, 141. doi: 10.3389/fnmol.2016.00141 PMID: 27999530
  14. Li, J.; He, P.; Lu, X.; Guo, Y.; Liu, M.; Li, G.; Ding, J. A resting-state functional magnetic resonance imaging study of whole-brain functional connectivity of voxel levels in patients with irritable bowel syndrome with depressive symptoms. J. Neurogastroenterol. Motil., 2021, 27(2), 248-256. doi: 10.5056/jnm20209 PMID: 33795543
  15. Martinou, E.; Stefanova, I.; Iosif, E.; Angelidi, A.M. Neurohormonal changes in the gut-brain axis and underlying neuroendocrine mechanisms following bariatric surgery. Int. J. Mol. Sci., 2022, 23(6), 3339. doi: 10.3390/ijms23063339 PMID: 35328759
  16. Carabotti, M.; Scirocco, A.; Maselli, M.A.; Severi, C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol., 2015, 28(2), 203-209. PMID: 25830558
  17. Muhammad, F.; Fan, B.; Wang, R.; Ren, J.; Jia, S.; Wang, L.; Chen, Z.; Liu, X.A. The molecular gut-brain axis in early brain development. Int. J. Mol. Sci., 2022, 23(23), 15389. doi: 10.3390/ijms232315389 PMID: 36499716
  18. Sarubbo, F.; Cavallucci, V.; Pani, G. The influence of gut microbiota on neurogenesis: Evidence and hopes. Cells, 2022, 11(3), 382. doi: 10.3390/cells11030382 PMID: 35159192
  19. Song, J.G.; Yu, M.S.; Lee, B.; Lee, J.; Hwang, S.H.; Na, D.; Kim, H.W. Analysis methods for the gut microbiome in neuropsychiatric and neurodegenerative disorders. Comput. Struct. Biotechnol. J., 2022, 20, 1097-1110. doi: 10.1016/j.csbj.2022.02.024 PMID: 35317228
  20. Wachsmuth, H.R.; Weninger, S.N.; Duca, F.A. Role of the gut–brain axis in energy and glucose metabolism. Exp. Mol. Med., 2022, 54(4), 377-392. doi: 10.1038/s12276-021-00677-w PMID: 35474341
  21. Chakrabarti, A.; Geurts, L.; Hoyles, L.; Iozzo, P.; Kraneveld, A.D.; La Fata, G.; Miani, M.; Patterson, E.; Pot, B.; Shortt, C.; Vauzour, D. The microbiota-gut-brain axis: Pathways to better brain health. Perspectives on what we know, what we need to investigate and how to put knowledge into practice. Cell. Mol. Life Sci., 2022, 79(2), 80. doi: 10.1007/s00018-021-04060-w PMID: 35044528
  22. Rutsch, A.; Kantsjö, J.B.; Ronchi, F. The gut-brain axis: How microbiota and host inflammasome influence brain physiology and pathology. Front. Immunol., 2020, 11, 604179. doi: 10.3389/fimmu.2020.604179 PMID: 33362788
  23. Karl, J.P.; Hatch, A.M.; Arcidiacono, S.M.; Pearce, S.C.; Feliciano, P.I.G.; Doherty, L.A.; Soares, J.W. Effects of psychological, environmental and physical stressors on the gut microbiota. Front. Microbiol., 2018, 9, 2013. doi: 10.3389/fmicb.2018.02013 PMID: 30258412
  24. Gebrayel, P.; Nicco, C.; Al Khodor, S.; Bilinski, J.; Caselli, E.; Comelli, E.M.; Egert, M.; Giaroni, C.; Karpinski, T.M.; Loniewski, I.; Mulak, A.; Reygner, J.; Samczuk, P.; Serino, M.; Sikora, M.; Terranegra, A.; Ufnal, M.; Villeger, R.; Pichon, C.; Konturek, P.; Edeas, M. Microbiota medicine: Towards clinical revolution. J. Transl. Med., 2022, 20(1), 111. doi: 10.1186/s12967-022-03296-9 PMID: 35255932
  25. Afzaal, M.; Saeed, F.; Shah, Y.A.; Hussain, M.; Rabail, R.; Socol, C.T.; Hassoun, A.; Pateiro, M.; Lorenzo, J.M.; Rusu, A.V.; Aadil, R.M. Human gut microbiota in health and disease: Unveiling the relationship. Front. Microbiol., 2022, 13, 999001. doi: 10.3389/fmicb.2022.999001 PMID: 36225386
  26. Chidambaram, S.B.; Essa, M.M.; Rathipriya, A.G.; Bishir, M.; Ray, B.; Mahalakshmi, A.M.; Tousif, A.H.; Sakharkar, M.K.; Kashyap, R.S.; Friedland, R.P.; Monaghan, T.M. Gut dysbiosis, defective autophagy and altered immune responses in neurodegenerative diseases: Tales of a vicious cycle. Pharmacol. Ther., 2022, 231, 107988. doi: 10.1016/j.pharmthera.2021.107988 PMID: 34536490
  27. Carding, S.; Verbeke, K.; Vipond, D.T.; Corfe, B.M.; Owen, L.J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis., 2015, 26, 26191. PMID: 25651997
  28. Scriven, M.; Dinan, T.; Cryan, J.; Wall, M. Neuropsychiatric disorders: Influence of gut microbe to brain signalling. Diseases, 2018, 6(3), 78. doi: 10.3390/diseases6030078 PMID: 30200574
  29. Sandhu, K.V.; Sherwin, E.; Schellekens, H.; Stanton, C.; Dinan, T.G.; Cryan, J.F. Feeding the microbiota-gut-brain axis: Diet, microbiome, and neuropsychiatry. Transl. Res., 2017, 179, 223-244. doi: 10.1016/j.trsl.2016.10.002 PMID: 27832936
  30. Socała, K.; Doboszewska, U.; Szopa, A.; Serefko, A.; Włodarczyk, M.; Zielińska, A.; Poleszak, E.; Fichna, J.; Wlaź, P. The role of microbiota-gut-brain axis in neuropsychiatric and neurological disorders. Pharmacol. Res., 2021, 172, 105840. doi: 10.1016/j.phrs.2021.105840 PMID: 34450312
  31. Zang, Y.; Lai, X.; Li, C.; Ding, D.; Wang, Y.; Zhu, Y. The role of gut microbiota in various neurological and psychiatric disorders-an evidence mapping based on quantified evidence. Mediators Inflamm., 2023, 2023, 1-16. doi: 10.1155/2023/5127157 PMID: 36816743
  32. Suganya, K.; Koo, B.S. Gut-brain axis: Role of gut microbiota on neurological disorders and how probiotics/prebiotics beneficially modulate microbial and immune pathways to improve brain functions. Int. J. Mol. Sci., 2020, 21(20), 7551. doi: 10.3390/ijms21207551 PMID: 33066156
  33. Abo-Shaban, T.; Sharna, S.S.; Hosie, S.; Lee, C.Y.Q.; Balasuriya, G.K.; McKeown, S.J.; Franks, A.E.; Yardin, H.E.L. Issues for patchy tissues: Defining roles for gut-associated lymphoid tissue in neurodevelopment and disease. J. Neural Transm., 2023, 130(3), 269-280. doi: 10.1007/s00702-022-02561-x PMID: 36309872
  34. Agustí, A.; Pardo, G.M.P.; Almela, L.I.; Campillo, I.; Maes, M.; Pérez, R.M.; Sanz, Y. Interplay between the gut-brain axis, obesity and cognitive function. Front. Neurosci., 2018, 12, 155. doi: 10.3389/fnins.2018.00155 PMID: 29615850
  35. Rudzki, L.; Maes, M. The microbiota-gut-immune-glia (MGIG) axis in major depression. Mol. Neurobiol., 2020, 57(10), 4269-4295. doi: 10.1007/s12035-020-01961-y PMID: 32700250
  36. Clapp, M.; Aurora, N.; Herrera, L.; Bhatia, M.; Wilen, E.; Wakefield, S. Gut microbiota’s effect on mental health: The gut-brain axis. Clin. Pract., 2017, 7(4), 987. doi: 10.4081/cp.2017.987 PMID: 29071061
  37. Berk, M.; Williams, L.J.; Jacka, F.N.; O’Neil, A.; Pasco, J.A.; Moylan, S.; Allen, N.B.; Stuart, A.L.; Hayley, A.C.; Byrne, M.L.; Maes, M. So depression is an inflammatory disease, but where does the inflammation come from? BMC Med., 2013, 11(1), 200. doi: 10.1186/1741-7015-11-200 PMID: 24228900
  38. Maes, M.; Vasupanrajit, A.; Jirakran, K.; Klomkliew, P.; Chanchaem, P.; Tunvirachaisakul, C.; Plaimas, K.; Suratanee, A.; Payungporn, S. Adverse childhood experiences and reoccurrence of illness impact the gut microbiome, which affects suicidal behaviours and the phenome of major depression: Towards enterotypic phenotypes. Acta Neuropsychiatr., 2023, 35(6), 328-345. doi: 10.1017/neu.2023.21 PMID: 37052305
  39. Maes, M.; Yirmyia, R.; Noraberg, J.; Brene, S.; Hibbeln, J.; Perini, G.; Kubera, M.; Bob, P.; Lerer, B.; Maj, M. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab. Brain Dis., 2009, 24(1), 27-53. doi: 10.1007/s11011-008-9118-1 PMID: 19085093
  40. Rudzki, L.; Maes, M. From "Leaky Gut" to impaired glia-neuron communication in depression. Adv. Exp. Med. Biol., 2021, 1305, 129-155. doi: 10.1007/978-981-33-6044-0_9 PMID: 33834399
  41. Martínez, R.S.; Real, S.L.; García, G.A.P.; Cruz, T.E.; Jonapa, C.L.A.; Amedei, A.; García, A.M.M. Neuroinflammation, microbiota-gut-brain axis, and depression: The vicious circle. J. Integr. Neurosci., 2023, 22(3), 65. doi: 10.31083/j.jin2203065 PMID: 37258450
  42. Qin, H.Y.; Cheng, C.W.; Tang, X.D.; Bian, Z.X. Impact of psychological stress on irritable bowel syndrome. World J. Gastroenterol., 2014, 20(39), 14126-14131. doi: 10.3748/wjg.v20.i39.14126 PMID: 25339801
  43. Belei, O.; Basaca, D.G.; Olariu, L.; Pantea, M.; Bozgan, D.; Nanu, A.; Sîrbu, I.; Mărginean, O.; Enătescu, I. The interaction between stress and inflammatory bowel disease in pediatric and adult patients. J. Clin. Med., 2024, 13(5), 1361. doi: 10.3390/jcm13051361 PMID: 38592680
  44. Howland, R.H. Vagus nerve stimulation. Curr. Behav. Neurosci. Rep., 2014, 1(2), 64-73. doi: 10.1007/s40473-014-0010-5 PMID: 24834378
  45. Berthoud, H.R.; Neuhuber, W.L. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci., 2000, 85(1-3), 1-17. doi: 10.1016/S1566-0702(00)00215-0 PMID: 11189015
  46. Forsythe, P.; Bienenstock, J.; Kunze, W.A. Vagal pathways for microbiome-brain-gut axis communication. Adv. Exp. Med. Biol., 2014, 817, 115-133. doi: 10.1007/978-1-4939-0897-4_5 PMID: 24997031
  47. Latorre, R.; Sternini, C.; Giorgio, D.R.; Meerveld, G.V.B. Enteroendocrine cells: A review of their role in brain–gut communication. Neurogastroenterol. Motil., 2016, 28(5), 620-630. doi: 10.1111/nmo.12754 PMID: 26691223
  48. Kanai, T.; Teratani, T. Role of the vagus nerve in the gut-brain axis: Development and maintenance of gut regulatory T cells via the liver-brain-gut vago-vagal reflex. Brain Nerve, 2022, 74(8), 971-977. PMID: 35941793
  49. Han, Y.; Wang, B.; Gao, H.; He, C.; Hua, R.; Liang, C.; Zhang, S.; Wang, Y.; Xin, S.; Xu, J. Vagus nerve and underlying impact on the gut microbiota-brain axis in behavior and neurodegenerative diseases. J. Inflamm. Res., 2022, 15, 6213-6230. doi: 10.2147/JIR.S384949 PMID: 36386584
  50. Chang, L.; Wei, Y.; Hashimoto, K. Brain–gut–microbiota axis in depression: A historical overview and future directions. Brain Res. Bull., 2022, 182, 44-56. doi: 10.1016/j.brainresbull.2022.02.004 PMID: 35151796
  51. Garg, K.; Mohajeri, M.H. Potential effects of the most prescribed drugs on the microbiota-gut-brain-axis: A review. Brain Res. Bull., 2024, 207, 110883. doi: 10.1016/j.brainresbull.2024.110883 PMID: 38244807
  52. Vich Vila, A.; Collij, V.; Sanna, S.; Sinha, T.; Imhann, F.; Bourgonje, A.R.; Mujagic, Z.; Jonkers, D.M.A.E.; Masclee, A.A.M.; Fu, J.; Kurilshikov, A.; Wijmenga, C.; Zhernakova, A.; Weersma, R.K. Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat. Commun., 2020, 11(1), 362. doi: 10.1038/s41467-019-14177-z PMID: 31953381
  53. Karakan, T.; Ozkul, C.; Akkol, K.E.; Bilici, S.; Sánchez, S.E.; Capasso, R. Gut-brain-microbiota axis: Antibiotics and functional gastrointestinal disorders. Nutrients, 2021, 13(2), 389. doi: 10.3390/nu13020389 PMID: 33513791
  54. Maier, L.; Pruteanu, M.; Kuhn, M.; Zeller, G.; Telzerow, A.; Anderson, E.E.; Brochado, A.R.; Fernandez, K.C.; Dose, H.; Mori, H.; Patil, K.R.; Bork, P.; Typas, A. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature, 2018, 555(7698), 623-628. doi: 10.1038/nature25979 PMID: 29555994
  55. Essmat, N.; Karádi, D.Á.; Zádor, F.; Király, K.; Fürst, S.; Khrasani, A.M. Insights into the current and possible future use of opioid antagonists in relation to opioid-induced constipation and dysbiosis. Molecules, 2023, 28(23), 7766. doi: 10.3390/molecules28237766 PMID: 38067494
  56. Bernabè, G.; Shalata, M.E.M.; Zatta, V.; Bellato, M.; Porzionato, A.; Castagliuolo, I.; Brun, P. Antibiotic treatment induces long-lasting effects on gut microbiota and the enteric nervous system in mice. Antibiotics, 2023, 12(6), 1000. doi: 10.3390/antibiotics12061000 PMID: 37370319
  57. Caparrós-Martín, J.A.; Lareu, R.R.; Ramsay, J.P.; Peplies, J.; Reen, F.J.; Headlam, H.A.; Ward, N.C.; Croft, K.D.; Newsholme, P.; Hughes, J.D.; O’Gara, F. Statin therapy causes gut dysbiosis in mice through a PXR-dependent mechanism. Microbiome, 2017, 5(1), 95. doi: 10.1186/s40168-017-0312-4 PMID: 28793934
  58. Doestzada, M.; Vila, A.V.; Zhernakova, A.; Koonen, D.P.Y.; Weersma, R.K.; Touw, D.J.; Kuipers, F.; Wijmenga, C.; Fu, J. Pharmacomicrobiomics: A novel route towards personalized medicine? Protein Cell, 2018, 9(5), 432-445. doi: 10.1007/s13238-018-0547-2 PMID: 29705929
  59. Crişan, I.M.; Dumitraşcu, D.L. Irritable bowel syndrome: Peripheral mechanisms and therapeutic implications. Clujul Med., 2014, 87(2), 73-79. PMID: 26528001
  60. Saha, L. Irritable bowel syndrome: Pathogenesis, diagnosis, treatment, and evidence-based medicine. World J. Gastroenterol., 2014, 20(22), 6759-6773. doi: 10.3748/wjg.v20.i22.6759 PMID: 24944467
  61. Weaver, K.R.; Melkus, G.D.E.; Henderson, W.A. Irritable bowel syndrome. Am. J. Nurs., 2017, 117(6), 48-55. doi: 10.1097/01.NAJ.0000520253.57459.01 PMID: 28541989
  62. Lee, Y.J.; Park, K.S. Irritable bowel syndrome: Emerging paradigm in pathophysiology. World J. Gastroenterol., 2014, 20(10), 2456-2469. doi: 10.3748/wjg.v20.i10.2456 PMID: 24627583
  63. Chong, P.P.; Chin, V.K.; Looi, C.Y.; Wong, W.F.; Madhavan, P.; Yong, V.C. The microbiome and irritable bowel syndrome - A review on the pathophysiology, current research and future therapy. Front. Microbiol., 2019, 10, 1136. doi: 10.3389/fmicb.2019.01136 PMID: 31244784
  64. Oka, P.; Parr, H.; Barberio, B.; Black, C.J.; Savarino, E.V.; Ford, A.C. Global prevalence of irritable bowel syndrome according to Rome III or IV criteria: A systematic review and meta-analysis. Lancet Gastroenterol. Hepatol., 2020, 5(10), 908-917. doi: 10.1016/S2468-1253(20)30217-X PMID: 32702295
  65. Camilleri, M. Diagnosis and treatment of irritable bowel syndrome: A review. JAMA, 2021, 325(9), 865-877. doi: 10.1001/jama.2020.22532 PMID: 33651094
  66. Dinic, R.B.; Rajkovic, T.S.; Grgov, S.; Petrovic, G.; Zivkovic, V. Irritable bowel syndrome - From etiopathogenesis to therapy. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub., 2018, 162(1), 1-9. doi: 10.5507/bp.2017.057 PMID: 29358788
  67. Rodiño-Janeiro, B.K.; Vicario, M.; Cotoner, A.C.; García, P.R.; Santos, J. A review of microbiota and irritable bowel syndrome: Future in therapies. Adv. Ther., 2018, 35(3), 289-310. doi: 10.1007/s12325-018-0673-5 PMID: 29498019
  68. Black, C.J.; Thakur, E.R.; Houghton, L.A.; Quigley, E.M.M.; Moayyedi, P.; Ford, A.C. Efficacy of psychological therapies for irritable bowel syndrome: Systematic review and network meta-analysis. Gut, 2020, 69(8), 1441-1451. doi: 10.1136/gutjnl-2020-321191 PMID: 32276950
  69. Grundmann, O.; Yoon, S.L. Irritable bowel syndrome: Epidemiology, diagnosis and treatment: An update for health‐care practitioners. J. Gastroenterol. Hepatol., 2010, 25(4), 691-699. doi: 10.1111/j.1440-1746.2009.06120.x PMID: 20074154
  70. Staudacher, H.M.; Walus, M.A.; Ford, A.C. Common mental disorders in irritable bowel syndrome: pathophysiology, management, and considerations for future randomised controlled trials. Lancet Gastroenterol. Hepatol., 2021, 6(5), 401-410. doi: 10.1016/S2468-1253(20)30363-0 PMID: 33587890
  71. Juruena, M.F.; Eror, F.; Cleare, A.J.; Young, A.H. The role of early life stress in HPA axis and anxiety. Adv. Exp. Med. Biol., 2020, 1191, 141-153. doi: 10.1007/978-981-32-9705-0_9 PMID: 32002927
  72. Distrutti, E.; Monaldi, L.; Ricci, P.; Fiorucci, S. Gut microbiota role in irritable bowel syndrome: New therapeutic strategies. World J. Gastroenterol., 2016, 22(7), 2219-2241. doi: 10.3748/wjg.v22.i7.2219 PMID: 26900286
  73. Occhipinti, K.; Smith, J. Irritable bowel syndrome: A review and update. Clin. Colon Rectal Surg., 2012, 25(1), 046-052. doi: 10.1055/s-0032-1301759 PMID: 23449495
  74. Kano, M.; Muratsubaki, T.; Van Oudenhove, L.; Morishita, J.; Yoshizawa, M.; Kohno, K.; Yagihashi, M.; Tanaka, Y.; Mugikura, S.; Dupont, P.; Ly, H.G.; Takase, K.; Kanazawa, M.; Fukudo, S. Altered brain and gut responses to corticotropin-releasing hormone (CRH) in patients with irritable bowel syndrome. Sci. Rep., 2017, 7(1), 12425. doi: 10.1038/s41598-017-09635-x PMID: 28963545
  75. Tarar, Z.I.; Farooq, U.; Zafar, Y.; Gandhi, M.; Raza, S.; Kamal, F.; Tarar, M.F.; Ghouri, Y.A. Burden of anxiety and depression among hospitalized patients with irritable bowel syndrome: A nationwide analysis. Ir. J. Med. Sci., 2023, 192(5), 2159-2166. doi: 10.1007/s11845-022-03258-6 PMID: 36593438
  76. Eijsbouts, C.; Zheng, T.; Kennedy, N.A.; Bonfiglio, F.; Anderson, C.A.; Moutsianas, L.; Holliday, J.; Shi, J.; Shringarpure, S.; Agee, M.; Aslibekyan, S.; Auton, A.; Bell, R.K.; Bryc, K.; Clark, S.K.; Elson, S.L.; Brant, K.; Fontanillas, P.; Furlotte, N.A.; Gandhi, P.M.; Heilbron, K.; Hicks, B.; Hinds, D.A.; Huber, K.E.; Jewett, E.M.; Jiang, Y.; Kleinman, A.; Lin, K-H.; Litterman, N.K.; Luff, M.K.; McCreight, J.C.; McIntyre, M.H.; McManus, K.F.; Mountain, J.L.; Mozaffari, S.V.; Nandakumar, P.; Noblin, E.S.; Northover, C.A.M.; O’Connell, J.; Petrakovitz, A.A.; Pitts, S.J.; Poznik, G.D.; Sathirapongsasuti, J.F.; Shastri, A.J.; Shelton, J.F.; Tian, C.; Tung, J.Y.; Tunney, R.J.; Vacic, V.; Wang, X.; Zare, A.S.; Voda, A-I.; Kashyap, P.; Chang, L.; Mayer, E.; Heitkemper, M.; Sayuk, G.S.; Kulka, R.T.; Ringel, Y.; Chey, W.D.; Eswaran, S.; Merchant, J.L.; Shulman, R.J.; Bujanda, L.; Etxebarria, G.K.; Dlugosz, A.; Lindberg, G.; Schmidt, P.T.; Karling, P.; Ohlsson, B.; Walter, S.; Faresjö, Å.O.; Simren, M.; Halfvarson, J.; Portincasa, P.; Barbara, G.; Satta, U.P.; Neri, M.; Nardone, G.; Cuomo, R.; Galeazzi, F.; Bellini, M.; Latiano, A.; Houghton, L.; Jonkers, D.; Kurilshikov, A.; Weersma, R.K.; Netea, M.; Tesarz, J.; Gauss, A.; Stengel, G.M.; Andresen, V.; Frieling, T.; Pehl, C.; Schaefert, R.; Niesler, B.; Lieb, W.; Hanevik, K.; Langeland, N.; Wensaas, K-A.; Litleskare, S.; Gabrielsen, M.E.; Thomas, L.; Thijs, V.; Lemmens, R.; Van Oudenhove, L.; Wouters, M.; Farrugia, G.; Franke, A.; Hübenthal, M.; Abecasis, G.; Zawistowski, M.; Skogholt, A.H.; Jensen, N.E.; Hveem, K.; Esko, T.; Laving, T.M.; Zhernakova, A.; Camilleri, M.; Boeckxstaens, G.; Whorwell, P.J.; Spiller, R.; McVean, G.; D’Amato, M.; Jostins, L.; Parkes, M. Genome-wide analysis of 53,400 people with irritable bowel syndrome highlights shared genetic pathways with mood and anxiety disorders. Nat. Genet., 2021, 53(11), 1543-1552. doi: 10.1038/s41588-021-00950-8 PMID: 34741163
  77. Aziz, M.; Kumar, J.; Nawawi, M.K.; Ali, R.R.; Mokhtar, N. Irritable bowel syndrome, depression, and neurodegeneration: A bidirectional communication from gut to brain. Nutrients, 2021, 13(9), 3061. doi: 10.3390/nu13093061 PMID: 34578939
  78. Midenfjord, I.; Polster, A.; Sjövall, H.; Törnblom, H.; Simrén, M. Anxiety and depression in irritable bowel syndrome: Exploring the interaction with other symptoms and pathophysiology using multivariate analyses. Neurogastroenterol. Motil., 2019, 31(8), e13619. doi: 10.1111/nmo.13619 PMID: 31056802
  79. Ng, Q.X.; Soh, A.Y.S.; Loke, W.; Venkatanarayanan, N.; Lim, D.Y.; Yeo, W.S. Systematic review with meta‐analysis: The association between post‐traumatic stress disorder and irritable bowel syndrome. J. Gastroenterol. Hepatol., 2019, 34(1), 68-73. doi: 10.1111/jgh.14446 PMID: 30144372
  80. Creed, F. Risk factors for self-reported irritable bowel syndrome with prior psychiatric disorder: The lifelines cohort study. J. Neurogastroenterol. Motil., 2022, 28(3), 442-453. doi: 10.5056/jnm21041 PMID: 35799238
  81. Fadgyas-Stanculete, M.; Buga, A.M.; Popa-Wagner, A.; Dumitrascu, D.L. The relationship between irritable bowel syndrome and psychiatric disorders: From molecular changes to clinical manifestations. J. Mol. Psychiatry, 2014, 2(1), 4. doi: 10.1186/2049-9256-2-4 PMID: 25408914
  82. Lydiard, R.B.; Falsetti, S.A. Experience with anxiety and depression treatment studies: implications for designing irritable bowel syndrome clinical trials. Am. J. Med., 1999, 107(5), 65-73. doi: 10.1016/S0002-9343(99)00082-0 PMID: 10588175
  83. Tao, E.; Long, G.; Yang, T.; Chen, B.; Guo, R.; Ye, D.; Fang, M.; Jiang, M. Maternal separation induced visceral hypersensitivity evaluated via novel and small size distention balloon in post-weaning mice. Front. Neurosci., 2022, 15, 803957. doi: 10.3389/fnins.2021.803957 PMID: 35153662
  84. Ge, L.; Liu, S.; Li, S.; Yang, J.; Hu, G.; Xu, C.; Song, W. Psychological stress in inflammatory bowel disease: Psychoneuroimmunological insights into bidirectional gut–brain communications. Front. Immunol., 2022, 13, 1016578. doi: 10.3389/fimmu.2022.1016578 PMID: 36275694
  85. Sun, Y.; Xie, R.; Li, L.; Jin, G.; Zhou, B.; Huang, H.; Li, M.; Yang, Y.; Liu, X.; Cao, X.; Wang, B.; Liu, W.; Jiang, K.; Cao, H. Prenatal maternal stress exacerbates experimental colitis of offspring in adulthood. Front. Immunol., 2021, 12, 700995. doi: 10.3389/fimmu.2021.700995 PMID: 34804005
  86. Császár-Nagy, N.; Bókkon, I. Mother-newborn separation at birth in hospitals: A possible risk for neurodevelopmental disorders? Neurosci. Biobehav. Rev., 2018, 84, 337-351. doi: 10.1016/j.neubiorev.2017.08.013 PMID: 28851575
  87. Bradford, K.; Shih, W.; Videlock, E.J.; Presson, A.P.; Naliboff, B.D.; Mayer, E.A.; Chang, L. Association between early adverse life events and irritable bowel syndrome. Clin. Gastroenterol. Hepatol., 2012, 10(4), 385-390.e1. doi: 10.1016/j.cgh.2011.12.018
  88. Chitkara, D.K.; van Tilburg, M.A.L.; Martin, B.N.; Whitehead, W.E. Early life risk factors that contribute to irritable bowel syndrome in adults: A systematic review. Am. J. Gastroenterol., 2008, 103(3), 765-774. doi: 10.1111/j.1572-0241.2007.01722.x PMID: 18177446
  89. Videlock, E.J.; Chang, L. Latest insights on the pathogenesis of irritable bowel syndrome. Gastroenterol. Clin. North Am., 2021, 50(3), 505-522. doi: 10.1016/j.gtc.2021.04.002 PMID: 34304785
  90. Tang, H.Y.; Jiang, A.J.; Wang, X.Y.; Wang, H.; Guan, Y.Y.; Li, F.; Shen, G.M. Uncovering the pathophysiology of irritable bowel syndrome by exploring the gut-brain axis: A narrative review. Ann. Transl. Med., 2021, 9(14), 1187. doi: 10.21037/atm-21-2779 PMID: 34430628
  91. Salhy, E.M. Irritable bowel syndrome: Diagnosis and pathogenesis. World J. Gastroenterol., 2012, 18(37), 5151-5163. doi: 10.3748/wjg.v18.i37.5151 PMID: 23066308
  92. Gieryńska, M.; Szulc-Dąbrowska, L.; Struzik, J.; Mielcarska, M.B.; Zboroch, G.K.P. Integrity of the intestinal barrier: the involvement of epithelial cells and microbiota-a mutual relationship. Animals, 2022, 12(2), 145. doi: 10.3390/ani12020145 PMID: 35049768
  93. Gritz, E.C.; Bhandari, V. The human neonatal gut microbiome: A brief review. Front Pediatr., 2015, 3, 17. PMID: 25798435
  94. Wu, H.J.; Wu, E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes, 2012, 3(1), 4-14. doi: 10.4161/gmic.19320 PMID: 22356853
  95. Ng, Q.X.; Soh, A.Y.S.; Loke, W.; Lim, D.Y.; Yeo, W.S. The role of inflammation in irritable bowel syndrome (IBS). J. Inflamm. Res., 2018, 11, 345-349. doi: 10.2147/JIR.S174982 PMID: 30288077
  96. Shi, N.; Li, N.; Duan, X.; Niu, H. Interaction between the gut microbiome and mucosal immune system. Mil. Med. Res., 2017, 4(1), 14. doi: 10.1186/s40779-017-0122-9 PMID: 28465831
  97. Lazaridis, N.; Germanidis, G. Current insights into the innate immune system dysfunction in irritable bowel syndrome. Ann. Gastroenterol., 2018, 31(2), 171-187. doi: 10.20524/aog.2018.0229 PMID: 29507464
  98. Akiho, H.; Ihara, E.; Nakamura, K. Low-grade inflammation plays a pivotal role in gastrointestinal dysfunction in irritable bowel syndrome. World J. Gastrointest. Pathophysiol., 2010, 1(3), 97-105. doi: 10.4291/wjgp.v1.i3.97 PMID: 21607147
  99. El-Hakim, Y.; Bake, S.; Mani, K.K.; Sohrabji, F. Impact of intestinal disorders on central and peripheral nervous system diseases. Neurobiol. Dis., 2022, 165, 105627. doi: 10.1016/j.nbd.2022.105627 PMID: 35032636
  100. Lu, S.; Jiang, H.; Shi, Y. Association between irritable bowel syndrome and Parkinson’s disease: A systematic review and meta‐analysis. Acta Neurol. Scand., 2022, 145(4), 442-448. doi: 10.1111/ane.13570 PMID: 34908158
  101. Yoon, S.Y.; Shin, J.; Heo, S.J.; Chang, J.S.; Sunwoo, M.K.; Kim, Y.W. Irritable bowel syndrome and subsequent risk of Parkinson’s disease: A nationwide population-based matched-cohort study. J. Neurol., 2022, 269(3), 1404-1412. doi: 10.1007/s00415-021-10688-2 PMID: 34255181
  102. Alvino, B.; Arianna, F.; Assunta, B.; Antonio, C.; Emanuele, D.; Giorgia, M.; Leonardo, S.; Daniele, S.; Renato, D.; Buscarinu, M.C.; Massimiliano, M.; Crisafulli, S.G.; Aurora, Z.; Nicoletti, G.C.; Marco, S.; Viola, B.; Francesco, P.; Marfia, A.G.; Grazia, S.; Valentina, S.; Davide, O.; Giovanni, S.; Gioacchino, T.; Gallo, A. Prevalence and predictors of bowel dysfunction in a large multiple sclerosis outpatient population: An Italian multicenter study. J. Neurol., 2022, 269(3), 1610-1617. Erratum in: Prevalence and predictors of bowel dysfunction in a large multiple sclerosis outpatient population: An Italian multicenter study. J. Neurol., 2022; 269(5): 2824-2825.
  103. Lee, Y.T.; Hu, L.Y.; Shen, C.C.; Huang, M.W.; Tsai, S.J.; Yang, A.C.; Hu, C.K.; Perng, C.L.; Huang, Y.S.; Hung, J.H. Risk of psychiatric disorders following irritable bowel syndrome: A nationwide population-based cohort study. PLoS One, 2015, 10(7), e0133283. doi: 10.1371/journal.pone.0133283 PMID: 26222511
  104. Meade, E.; Garvey, M. The Role of neuro-immune interaction in chronic pain conditions; Functional somatic syndrome, neurogenic inflammation, and peripheral neuropathy. Int. J. Mol. Sci., 2022, 23(15), 8574. doi: 10.3390/ijms23158574 PMID: 35955708
  105. Frauches, B.A.C.; Boesmans, W. The enteric nervous system: The hub in a star network. Nat. Rev. Gastroenterol. Hepatol., 2020, 17(12), 717-718. doi: 10.1038/s41575-020-00377-2 PMID: 33087897
  106. Holland, A.M.; Frauches, B.A.C.; Keszthelyi, D.; Melotte, V.; Boesmans, W. The enteric nervous system in gastrointestinal disease etiology. Cell. Mol. Life Sci., 2021, 78(10), 4713-4733. doi: 10.1007/s00018-021-03812-y PMID: 33770200
  107. Nagy, N.; Goldstein, A.M. Enteric nervous system development: A crest cell’s journey from neural tube to colon. Semin. Cell Dev. Biol., 2017, 66, 94-106. doi: 10.1016/j.semcdb.2017.01.006 PMID: 28087321
  108. Gershon, M.D.; Ratcliffe, E.M. Developmental biology of the enteric nervous system: Pathogenesis of Hirschsprung’s disease and other congenital dysmotilities. Semin. Pediatr. Surg., 2004, 13(4), 224-235. doi: 10.1053/j.sempedsurg.2004.10.019 PMID: 15660316
  109. Torroglosa, A.; Alves, M.M.; Fernández, R.M.; Antiñolo, G.; Hofstra, R.M.; Borrego, S. Epigenetics in ENS development and Hirschsprung disease. Dev. Biol., 2016, 417(2), 209-216. doi: 10.1016/j.ydbio.2016.06.017 PMID: 27321561
  110. de Jonge, W.J. The gut’s little brain in control of intestinal immunity. ISRN Gastroenterol., 2013, 2013, 1-17. doi: 10.1155/2013/630159 PMID: 23691339
  111. Yang, X.; Lou, J.; Shan, W.; Ding, J.; Jin, Z.; Hu, Y.; Du, Q.; Liao, Q.; Xie, R.; Xu, J. Pathophysiologic role of neurotransmitters in digestive diseases. Front. Physiol., 2021, 12, 567650. doi: 10.3389/fphys.2021.567650 PMID: 34194334
  112. Spencer, N.J.; Travis, L.; Wiklendt, L.; Costa, M.; Hibberd, T.J.; Brookes, S.J.; Dinning, P.; Hu, H.; Wattchow, D.A.; Sorensen, J. Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice. Commun. Biol., 2021, 4(1), 955. doi: 10.1038/s42003-021-02485-4 PMID: 34376798
  113. Annahazi, A.; Schemann, M. The enteric nervous system: "A little brain in the gut". Neuroforum, 2020, 26(1), 31-42. doi: 10.1515/nf-2019-0027
  114. Schemann, M.; Frieling, T.; Enck, P. To learn, to remember, to forget—How smart is the gut? Acta Physiol., 2020, 228(1), e13296. doi: 10.1111/apha.13296 PMID: 31063665
  115. Furness, J.B.; Clerc, N.; Kunze, W.A. Memory in the enteric nervous system. Gut, 2000, 47(S4), 60-62. doi: 10.1136/gut.47.suppl_4.iv60
  116. Cheng, L. Progress on the regulation of DNA methylation in the development of the enteric nervous system. Int. J. Pediatr., 2018, 6, 756-760.
  117. Jaroy, E.G.; Acosta-Jimenez, L.; Hotta, R.; Goldstein, A.M.; Emblem, R.; Klungland, A.; Ougland, R. "Too much guts and not enough brains": (epi)genetic mechanisms and future therapies of Hirschsprung disease — A review. Clin. Epigenetics, 2019, 11(1), 135. doi: 10.1186/s13148-019-0718-x PMID: 31519213
  118. Uribe, R.A. Genetic regulation of enteric nervous system development in zebrafish. Biochem. Soc. Trans., 2024, 52(1), 177-190. doi: 10.1042/BST20230343 PMID: 38174765
  119. Kenny, S.E.; Tam, P.K.H.; Barcelo, G.M. Hirschsprung’s disease. Semin. Pediatr. Surg., 2010, 19(3), 194-200. doi: 10.1053/j.sempedsurg.2010.03.004 PMID: 20610192
  120. Diposarosa, R.; Bustam, N.A.; Sahiratmadja, E.; Susanto, P.S.; Sribudiani, Y. Literature review: Enteric nervous system development, genetic and epigenetic regulation in the etiology of Hirschsprung’s disease. Heliyon, 2021, 7(6), e07308. doi: 10.1016/j.heliyon.2021.e07308 PMID: 34195419
  121. Brosens, E.; Burns, A.J.; Brooks, A.S.; Matera, I.; Borrego, S.; Ceccherini, I.; Tam, P.K.; Barceló, G.M.M.; Thapar, N.; Benninga, M.A.; Hofstra, R.M.W.; Alves, M.M. Genetics of enteric neuropathies. Dev. Biol., 2016, 417(2), 198-208. doi: 10.1016/j.ydbio.2016.07.008 PMID: 27426273
  122. Torroglosa, A.; Villalba-Benito, L.; Toro, L.B.; Fernández, R.M.; Antiñolo, G.; Borrego, S. Epigenetic mechanisms in hirschsprung disease. Int. J. Mol. Sci., 2019, 20(13), 3123. doi: 10.3390/ijms20133123 PMID: 31247956
  123. Heanue, T.A.; Shepherd, I.T.; Burns, A.J. Enteric nervous system development in avian and zebrafish models. Dev. Biol., 2016, 417(2), 129-138. doi: 10.1016/j.ydbio.2016.05.017 PMID: 27235814
  124. Kuil, L.E.; Chauhan, R.K.; Cheng, W.W.; Hofstra, R.M.W.; Alves, M.M. Zebrafish: A model organism for studying enteric nervous system development and disease. Front. Cell Dev. Biol., 2021, 8, 629073. doi: 10.3389/fcell.2020.629073 PMID: 33553169
  125. Ganz, J.; Melancon, E.; Wilson, C.; Amores, A.; Batzel, P.; Strader, M.; Braasch, I.; Diba, P.; Kuhlman, J.A.; Postlethwait, J.H.; Eisen, J.S. Epigenetic factors Dnmt1 and Uhrf1 coordinate intestinal development. Dev. Biol., 2019, 455(2), 473-484. doi: 10.1016/j.ydbio.2019.08.002 PMID: 31394080
  126. Feng, G.; Sun, Y. The Polycomb group gene rnf2 is essential for central and enteric neural system development in zebrafish. Front. Neurosci., 2022, 16, 960149. doi: 10.3389/fnins.2022.960149 PMID: 36117635
  127. Liu, J.; Tan, Y.; Cheng, H.; Zhang, D.; Feng, W.; Peng, C. Functions of gut microbiota metabolites, current status and future perspectives. Aging Dis., 2022, 13(4), 1106-1126. doi: 10.14336/AD.2022.0104 PMID: 35855347
  128. Fujisaka, S.; Watanabe, Y.; Tobe, K. The gut microbiome: A core regulator of metabolism. J. Endocrinol., 2023, 256(3), e220111. doi: 10.1530/JOE-22-0111 PMID: 36458804
  129. Ansari, M.H.R.; Saher, S.; Parveen, R.; Khan, W.; Khan, I.A.; Ahmad, S. Role of gut microbiota metabolism and biotransformation on dietary natural products to human health implications with special reference to biochemoinformatics approach. J. Tradit. Complement. Med., 2023, 13(2), 150-160. doi: 10.1016/j.jtcme.2022.03.005 PMID: 36970455
  130. Swer, N.M.; Venkidesh, B.S.; Murali, T.S.; Mumbrekar, K.D. Gut microbiota-derived metabolites and their importance in neurological disorders. Mol. Biol. Rep., 2023, 50(2), 1663-1675. doi: 10.1007/s11033-022-08038-0 PMID: 36399245
  131. Yeramilli, V.; Cheddadi, R.; Shah, J.; Brawner, K.; Martin, C. A Review of the impact of maternal prenatal stress on offspring microbiota and metabolites. Metabolites, 2023, 13(4), 535. doi: 10.3390/metabo13040535 PMID: 37110193
  132. Mepham, J.; McGee, N.T.; Andrews, K.; Gonzalez, A. Exploring the effect of prenatal maternal stress on the microbiomes of mothers and infants: A systematic review. Dev. Psychobiol., 2023, 65(7), e22424. doi: 10.1002/dev.22424 PMID: 37860905
  133. Yang, H.; Guo, R.; Li, S.; Liang, F.; Tian, C.; Zhao, X.; Long, Y.; Liu, F.; Jiang, M.; Zhang, Y.; Ma, J.; Peng, M.; Zhang, S.; Ye, W.; Gan, Q.; Zeng, F.; Mao, S.; Liang, Q.; Ma, X.; Han, M.; Gao, F.; Yang, R.; Zhang, C.; Xiao, L.; Qin, J.; Li, S.; Zhu, C. Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity. NPJ Biofilms Microbiomes, 2020, 6(1), 32. doi: 10.1038/s41522-020-00142-y PMID: 32917878
  134. Gorczyca, K.; Obuchowska, A.; Trojnar, K.Ż.; Opoka, W.M.; Gorzelak, L.B. Changes in the gut microbiome and pathologies in pregnancy. Int. J. Environ. Res. Public Health, 2022, 19(16), 9961. doi: 10.3390/ijerph19169961 PMID: 36011603
  135. Srinivasan, K.; Satyanarayana, V.A.; Lukose, A. Maternal mental health in pregnancy and child behavior. Indian J. Psychiatry, 2011, 53(4), 351-361. doi: 10.4103/0019-5545.91911 PMID: 22303046
  136. Tuovinen, S.; Pulkkinen, L.M.; Girchenko, P.; Heinonen, K.; Lahti, J.; Reynolds, R.M.; Hämäläinen, E.; Villa, P.M.; Kajantie, E.; Laivuori, H.; Raikkonen, K. Maternal antenatal stress and mental and behavioral disorders in their children. J. Affect. Disord., 2021, 278, 57-65. doi: 10.1016/j.jad.2020.09.063 PMID: 32950844
  137. Van den Bergh, B.R.H.; van den Heuvel, M.I.; Lahti, M.; Braeken, M.; de Rooij, S.R.; Entringer, S.; Hoyer, D.; Roseboom, T.; Räikkönen, K.; King, S.; Schwab, M. Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci. Biobehav. Rev., 2020, 117, 26-64. doi: 10.1016/j.neubiorev.2017.07.003 PMID: 28757456
  138. Sulkowska, S.E.M. The impact of maternal gut microbiota during pregnancy on fetal gut-brain axis development and life-long health outcomes. Microorganisms, 2023, 11(9), 2199. doi: 10.3390/microorganisms11092199 PMID: 37764043
  139. Rusch, J.A.; Layden, B.T.; Dugas, L.R. Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis. Front. Endocrinol., 2023, 14, 1130689. doi: 10.3389/fendo.2023.1130689 PMID: 37404311
  140. Misiak, B.; Łoniewski, I.; Marlicz, W.; Frydecka, D.; Szulc, A.; Rudzki, L.; Samochowiec, J. The HPA axis dysregulation in severe mental illness: Can we shift the blame to gut microbiota? Prog. Neuropsychopharmacol. Biol. Psychiatry, 2020, 102, 109951. doi: 10.1016/j.pnpbp.2020.109951 PMID: 32335265
  141. Turroni, F.; Rizzo, S.M.; Ventura, M.; Bernasconi, S. Cross-talk between the infant/maternal gut microbiota and the endocrine system: A promising topic of research. Microbiome Res Rep., 2022, 1(2), 14. doi: 10.20517/mrr.2021.14 PMID: 38045647
  142. Garzoni, L.; Faure, C.; Frasch, M.G. Fetal cholinergic anti-inflammatory pathway and necrotizing enterocolitis: The brain-gut connection begins in utero. Front. Integr. Nuerosci., 2013, 7, 57. doi: 10.3389/fnint.2013.00057 PMID: 23964209
  143. Zijlmans, M.A.C.; Korpela, K.; Walraven, R.J.M.; de Vos, W.M.; de Weerth, C. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology, 2015, 53, 233-245. doi: 10.1016/j.psyneuen.2015.01.006 PMID: 25638481
  144. Gur, T.L.; Palkar, A.V.; Rajasekera, T.; Allen, J.; Niraula, A.; Godbout, J.; Bailey, M.T. Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring. Behav. Brain Res., 2019, 359, 886-894. doi: 10.1016/j.bbr.2018.06.025 PMID: 29949734
  145. Silva, Y.P.; Bernardi, A.; Frozza, R.L. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front. Endocrinol., 2020, 11, 25. doi: 10.3389/fendo.2020.00025 PMID: 32082260
  146. Dalile, B.; Vervliet, B.; Bergonzelli, G.; Verbeke, K.; Oudenhove, V.L. Colon-delivered short-chain fatty acids attenuate the cortisol response to psychosocial stress in healthy men: A randomized, placebo-controlled trial. Neuropsychopharmacology, 2020, 45(13), 2257-2266. doi: 10.1038/s41386-020-0732-x PMID: 32521538
  147. Zhang, D.; Jian, Y.P.; Zhang, Y.N.; Li, Y.; Gu, L.T.; Sun, H.H.; Liu, M.D.; Zhou, H.L.; Wang, Y.S.; Xu, Z.X. Short-chain fatty acids in diseases. Cell Commun. Signal., 2023, 21(1), 212. doi: 10.1186/s12964-023-01219-9 PMID: 37596634
  148. Chen, B.; Sun, L.; Zhang, X. Integration of microbiome and epigenome to decipher the pathogenesis of autoimmune diseases. J. Autoimmun., 2017, 83, 31-42. doi: 10.1016/j.jaut.2017.03.009 PMID: 28342734
  149. Li, L.; Zhao, S.; Xiang, T.; Feng, H.; Ma, L.; Fu, P. Epigenetic connection between gut microbiota-derived short-chain fatty acids and chromatin histone modification in kidney diseases. Chin. Med. J., 2022, 135(14), 1692-1694. doi: 10.1097/CM9.0000000000002295 PMID: 36193977
  150. Stein, R.A.; Riber, L. Epigenetic effects of short-chain fatty acids from the large intestine on host cells. Microlife, 2023, 4, uqad032.
  151. Woo, V.; Alenghat, T. Epigenetic regulation by gut microbiota. Gut Microbes, 2022, 14(1), 2022407. doi: 10.1080/19490976.2021.2022407 PMID: 35000562
  152. Yang, L.L.; Millischer, V.; Rodin, S.; MacFabe, D.F.; Villaescusa, J.C.; Lavebratt, C. Enteric short‐chain fatty acids promote proliferation of human neural progenitor cells. J. Neurochem., 2020, 154(6), 635-646. doi: 10.1111/jnc.14928 PMID: 31784978
  153. Kimura, I.; Miyamoto, J.; Kitano, O.R.; Watanabe, K.; Yamada, T.; Onuki, M.; Aoki, R.; Isobe, Y.; Kashihara, D.; Inoue, D.; Inaba, A.; Takamura, Y.; Taira, S.; Kumaki, S.; Watanabe, M.; Ito, M.; Nakagawa, F.; Irie, J.; Kakuta, H.; Shinohara, M.; Iwatsuki, K.; Tsujimoto, G.; Ohno, H.; Arita, M.; Itoh, H.; Hase, K. Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science, 2020, 367(6481), eaaw8429. doi: 10.1126/science.aaw8429 PMID: 32108090
  154. Liu, R.T. Childhood adversities and depression in adulthood: Current findings and future directions. Clin. Psychol. Sci. Pract., 2017, 24(2), 140-153. doi: 10.1111/cpsp.12190 PMID: 28924333
  155. Garcia-Rizo, C.; Bitanihirwe, B.K.Y. Implications of early life stress on fetal metabolic programming of schizophrenia: A focus on epiphenomena underlying morbidity and early mortality. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2020, 101, 109910. doi: 10.1016/j.pnpbp.2020.109910 PMID: 32142745
  156. Kwon, E.J.; Kim, Y.J. What is fetal programming?: A lifetime health is under the control of in utero health. Obstet. Gynecol. Sci., 2017, 60(6), 506-519. doi: 10.5468/ogs.2017.60.6.506 PMID: 29184858
  157. Gluckma, P.D.; Hanson, M.A. Predictive adaptive responses and human disease. In: The fetal matrix. Evolution, development and disease Cambridge; Cambridge Universiy Press: UK, 2005; pp. 78-102.
  158. Zietlow, A.L.; Nonnenmacher, N.; Reck, C.; Ditzen, B.; Müller, M. Emotional stress during pregnancy - Associations with maternal anxiety disorders, infant cortisol reactivity, and mother-child interaction at pre-school age. Front. Psychol., 2019, 10, 2179. doi: 10.3389/fpsyg.2019.02179 PMID: 31607996
  159. Howerton, C.L.; Bale, T.L. Prenatal programing: At the intersection of maternal stress and immune activation. Horm. Behav., 2012, 62(3), 237-242. doi: 10.1016/j.yhbeh.2012.03.007 PMID: 22465455
  160. Van den Bergh, B.R.H.; Van Calster, B.; Smits, T.; Van Huffel, S.; Lagae, L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology, 2008, 33(3), 536-545. doi: 10.1038/sj.npp.1301450 PMID: 17507916
  161. Begum, N.; Mandhare, A.; Tryphena, K.P.; Srivastava, S.; Shaikh, M.F.; Singh, S.B.; Khatri, D.K. Epigenetics in depression and gut-brain axis: A molecular crosstalk. Front. Aging Neurosci., 2022, 14, 1048333. doi: 10.3389/fnagi.2022.1048333 PMID: 36583185
  162. Li, D.; Li, Y.; Yang, S.; Lu, J.; Jin, X.; Wu, M. Diet-gut microbiota-epigenetics in metabolic diseases: From mechanisms to therapeutics. Biomed. Pharmacother., 2022, 153, 113290. doi: 10.1016/j.biopha.2022.113290 PMID: 35724509
  163. O’Riordan, K.J.; Collins, M.K.; Moloney, G.M.; Knox, E.G.; Aburto, M.R.; Fülling, C.; Morley, S.J.; Clarke, G.; Schellekens, H.; Cryan, J.F. Short chain fatty acids: Microbial metabolites for gut-brain axis signalling. Mol. Cell. Endocrinol., 2022, 546, 111572. doi: 10.1016/j.mce.2022.111572 PMID: 35066114
  164. Walker, R.W.; Clemente, J.C.; Peter, I.; Loos, R.J.F. The prenatal gut microbiome: Are we colonized with bacteria in utero? Pediatr. Obes., 2017, 2017(12 (S1)), 3-17. doi: 10.1111/ijpo.12217
  165. Nuriel-Ohayon, M.; Neuman, H.; Koren, O. Microbial changes during pregnancy, birth, and infancy. Front. Microbiol., 2016, 7, 1031. doi: 10.3389/fmicb.2016.01031 PMID: 27471494
  166. Aagaard, K.; Ma, J.; Antony, K.M.; Ganu, R.; Petrosino, J.; Versalovic, J. The placenta harbors a unique microbiome. Sci. Transl. Med., 2014, 6(237), 237ra65. doi: 10.1126/scitranslmed.3008599 PMID: 24848255
  167. Miko, E.; Csaszar, A.; Bodis, J.; Kovacs, K. The maternal-fetal gut microbiota axis: Physiological changes, dietary influence, and modulation possibilities. Life, 2022, 12(3), 424. doi: 10.3390/life12030424 PMID: 35330175

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