Display options
Share it on

Adv Neurobiol. 2021;26:283-313. doi: 10.1007/978-3-030-77375-5_12.

Brain Volume Loss, Astrocyte Reduction, and Inflammation in Anorexia Nervosa.

Advances in neurobiology

Jochen Seitz, Stefanie Trinh, Vanessa Kogel, Cordian Beyer

Affiliations

  1. Clinic of Child and Adolescent Psychiatry, University Hospital RWTH Aachen, Aachen, Germany. [email protected].
  2. Clinic of Child and Adolescent Psychiatry, University Hospital RWTH Aachen, Aachen, Germany.

PMID: 34888839 DOI: 10.1007/978-3-030-77375-5_12

Abstract

Anorexia nervosa is the third most common chronic disease in adolescence and is characterized by low body weight, body image distortion, weight phobia, and severe somatic consequences. Among the latter, marked brain volume reduction has been linked to astrocyte cell count reduction of about 50% in gray and white matter, while neuronal and other glial cell counts remain normal. Exact underlying mechanisms remain elusive; however, first results point to important roles of the catabolic state and the very low gonadal steroid hormones in these patients. They also appear to involve inflammatory states of "hungry astrocytes" and interactions with the gut microbiota. Functional impairments could affect the role of astrocytes in supporting neurons metabolically, neurotransmitter reuptake, and synapse formation, among others. These could be implicated in reduced learning, mood alterations, and sleep disturbances often seen in patients with AN and help explain their rigidity and difficulties in relearning processes in psychotherapy during starvation.

© 2021. The Author(s), under exclusive license to Springer Nature Switzerland AG.

Keywords: Activated astrocytes; Activity-based anorexia; Anorexia nervosa; Astrocyte cell count; Brain volume reduction; Gonadal steroid hormone reduction; Gut-brain axis; Inflammation; Microbiota; Neurocognitive deficits

References

  1. Abe T, Takahashi S, Suzuki N (2006) Oxidative metabolism in cultured rat astroglia: effects of reducing the glucose concentration in the culture medium and of D-aspartate or potassium stimulation. J Cerebral Blood Flow Metab 26:153–160. https://doi.org/10.1038/sj.jcbfm.9600175 - PubMed
  2. Agnello E et al (2012) Tumour necrosis factor alpha and oxidative stress as maintaining factors in the evolution of anorexia nervosa. Eat Weight Disord 17:e194–e199. https://doi.org/10.1007/bf03325347 - PubMed
  3. Allard C et al (2014) Hypothalamic astroglial connexins are required for brain glucose sensing-induced insulin secretion. J Cerebral Blood Flow Metab 34:339–346. https://doi.org/10.1038/jcbfm.2013.206 - PubMed
  4. Allende LM et al (1998) Immunodeficiency associated with anorexia nervosa is secondary and improves after refeeding. Immunology 94:543–551. https://doi.org/10.1046/j.1365-2567.1998.00548.x - PubMed
  5. Almeida A et al (2019) A new genomic blueprint of the human gut microbiota. Nature 568:499–504. https://doi.org/10.1038/s41586-019-0965-1 - PubMed
  6. Ananthakrishnan AN (2015) Epidemiology and risk factors for IBD nature reviews. Gastroenterol Hepatol 12:205–217. https://doi.org/10.1038/nrgastro.2015.34 - PubMed
  7. Aoki C, Wable G, Chowdhury TG, Sabaliauskas NA, Laurino K, Barbarich-Marsteller NC (2014) α4βδ-GABAARs in the hippocampal CA1 as a biomarker for resilience to activity-based anorexia. Neuroscience 265:108–123. https://doi.org/10.1016/j.neuroscience.2014.01.011 - PubMed
  8. Araújo GW, Beyer C, Arnold S (2008) Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J Neuroendocrinol 20:930–941. https://doi.org/10.1111/j.1365-2826.2008.01747.x - PubMed
  9. Arnold S, de Araújo GW, Beyer C (2008) Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones. J Mol Endocrinol 41:289–300. https://doi.org/10.1677/jme-08-0085 - PubMed
  10. Arumugam M et al (2011) Enterotypes of the human gut microbiome. Nature 473:174–180. https://doi.org/10.1038/nature09944 - PubMed
  11. Asano Y et al (2012) Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol 303:G1288–G1295. https://doi.org/10.1152/ajpgi.00341.2012 - PubMed
  12. Azcoitia I, Santos-Galindo M, Arevalo MA, Garcia-Segura LM (2010) Role of astroglia in the neuroplastic and neuroprotective actions of estradiol. Eur J Neurosci 32:1995–2002. https://doi.org/10.1111/j.1460-9568.2010.07516.x - PubMed
  13. Banasr M, Dwyer JM, Duman RS (2011) Cell atrophy and loss in depression: reversal by antidepressant treatment. Curr Opin Cell Biol 23:730–737. https://doi.org/10.1016/j.ceb.2011.09.002 - PubMed
  14. Barbarich-Marsteller NC et al (2013) Activity-based anorexia is associated with reduced hippocampal cell proliferation in adolescent female rats. Behav Brain Res 236:251–257. https://doi.org/10.1016/j.bbr.2012.08.047 - PubMed
  15. Belmonte L et al (2016) A role for intestinal TLR4-driven inflammatory response during activity-based anorexia. Sci Rep 6:35813. https://doi.org/10.1038/srep35813 - PubMed
  16. Boghi A, Sterpone S, Sales S, D’Agata F, Bradac GB, Zullo G, Munno D (2011) In vivo evidence of global and focal brain alterations in anorexia nervosa. Psychiatry Res 192:154–159. https://doi.org/10.1016/j.pscychresns.2010.12.008 - PubMed
  17. Böhm M, Papezova H, Hansikova H, Wenchich L, Zeman J (2007) Activities of respiratory chain complexes in isolated platelets in females with anorexia nervosa. Int J Eat Disord 40:659–663. https://doi.org/10.1002/eat.20403 - PubMed
  18. Brambilla F, Monti D, Franceschi C (2001) Plasma concentrations of interleukin-1-beta, interleukin-6 and tumor necrosis factor-alpha, and of their soluble receptors and receptor antagonist in anorexia nervosa. Psychiatry Res 103:107–114. https://doi.org/10.1016/s0165-1781(01)00283-9 - PubMed
  19. Brambilla R et al (2005) Inhibition of astroglial nuclear factor κB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 202:145–156. https://doi.org/10.1084/jem.20041918 - PubMed
  20. Brambilla F, Santonastaso P, Caregaro L, Favaro A (2018) Growth hormone and insulin-like growth factor 1 secretions in eating disorders: correlations with psychopathological aspects of the disorders. Psychiatry Res 263:233–237. https://doi.org/10.1016/j.psychres.2017.07.049 - PubMed
  21. Breit S, Kupferberg A, Rogler G, Hasler G (2018) Vagus nerve as modulator of the brain-gut axis in psychiatric and inflammatory disorders. Front Psych 9:44. https://doi.org/10.3389/fpsyt.2018.00044 - PubMed
  22. Breton J et al (2020) Gut microbiota alteration in a mouse model of anorexia nervosa. Clin Nutr (Edinburgh, Scotland). https://doi.org/10.1016/j.clnu.2020.05.002 - PubMed
  23. Brotfain E, Gruenbaum SE, Boyko M, Kutz R, Zlotnik A, Klein M (2016) Neuroprotection by estrogen and progesterone in traumatic brain injury and spinal cord injury. Curr Neuropharmacol 14:641–653. https://doi.org/10.2174/1570159x14666160309123554 - PubMed
  24. Buhren K et al (2014) Comorbid psychiatric disorders in female adolescents with first-onset anorexia nervosa. Europ Eating Disord Rev 22:39–44. https://doi.org/10.1002/erv.2254 - PubMed
  25. Caruso C, Carniglia L, Durand D, Gonzalez PV, Scimonelli TN, Lasaga M (2012) Melanocortin 4 receptor activation induces brain-derived neurotrophic factor expression in rat astrocytes through cyclic AMP-protein kinase A pathway. Mol Cell Endocrinol 348:47–54. https://doi.org/10.1016/j.mce.2011.07.036 - PubMed
  26. Caso JR et al (2020) Dysfunction of inflammatory pathways in adolescent female patients with anorexia nervosa. Prog Neuro-Psychopharmacol Biol Psychiatry 96:109727. https://doi.org/10.1016/j.pnpbp.2019.109727 - PubMed
  27. Castro-Fornieles J et al (2010) A cross-sectional and follow-up functional MRI study with a working memory task in adolescent anorexia nervosa. Neuropsychologia 48:4111–4116. https://doi.org/10.1016/j.neuropsychologia.2010.10.003 - PubMed
  28. Cekanaviciute E, Buckwalter MS (2016) Astrocytes: integrative regulators of Neuroinflammation in stroke and other neurological diseases. Neurotherapeutics 13:685–701. https://doi.org/10.1007/s13311-016-0477-8 - PubMed
  29. Chandel NS, Trzyna WC, McClintock DS, Schumacker PT (2000) Role of oxidants in NF-κB activation and TNF-α gene transcription induced by hypoxia and endotoxin. J Immunol 165:1013–1021. https://doi.org/10.4049/jimmunol.165.2.1013 - PubMed
  30. Chen Y, Swanson RA (2003) Astrocytes and brain injury. J Cerebral Blood Flow Metab 23:137–149. https://doi.org/10.1097/01.Wcb.0000044631.80210.3c - PubMed
  31. Chen JQ, Cammarata PR, Baines CP, Yager JD (2009) Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta 1793:1540–1570. https://doi.org/10.1016/j.bbamcr.2009.06.001 - PubMed
  32. Chen Y, Zhang J, Tan H, Li J, Yu Y (2020) Detrimental effects of hypercortisolism on brain structure and related risk factors. Sci Rep 10:12708. https://doi.org/10.1038/s41598-020-68166-0 - PubMed
  33. Choi SS, Lee HJ, Lim I, Satoh J-I, Kim SU (2014) Human astrocytes: secretome profiles of cytokines and chemokines. PLoS One 9:e92325–e92325. https://doi.org/10.1371/journal.pone.0092325 - PubMed
  34. Chui HT et al (2008) Cognitive function and brain structure in females with a history of adolescent-onset anorexia nervosa. Pediatrics 122:e426–e437. https://doi.org/10.1542/peds.2008-0170 - PubMed
  35. Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG (2014) Minireview: gut microbiota: the neglected endocrine organ. Mol Endocrinol (Baltimore, MD) 28:1221–1238. https://doi.org/10.1210/me.2014-1108 - PubMed
  36. Colombo E et al (2012) Stimulation of the neurotrophin receptor TrkB on astrocytes drives nitric oxide production and neurodegeneration. J Exp Med 209:521–535. https://doi.org/10.1084/jem.20110698 - PubMed
  37. Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712. https://doi.org/10.1038/nrn3346 - PubMed
  38. Dalton B et al (2018) A meta-analysis of cytokine concentrations in eating disorders. J Psychiatr Res 103:252–264. https://doi.org/10.1016/j.jpsychires.2018.06.002 - PubMed
  39. Dalton B, Leppanen J, Campbell IC, Chung R, Breen G, Schmidt U, Himmerich H (2020) A longitudinal analysis of cytokines in anorexia nervosa. Brain Behav Immun 85:88–95. https://doi.org/10.1016/j.bbi.2019.05.012 - PubMed
  40. Darby A, Hay P, Mond J, Quirk F, Buttner P, Kennedy L (2009) The rising prevalence of comorbid obesity and eating disorder behaviors from 1995 to 2005. Int J Eat Disord 42:104–108. https://doi.org/10.1002/eat.20601 - PubMed
  41. Derrien M, Belzer C, de Vos WM (2017) Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 106:171–181. https://doi.org/10.1016/j.micpath.2016.02.005 - PubMed
  42. Dmitrzak-Weglarz M et al (2013) Serum neurotrophin concentrations in polish adolescent girls with anorexia nervosa. Neuropsychobiology 67:25–32. https://doi.org/10.1159/000343500 - PubMed
  43. Dorrington MG, Fraser IDC (2019) NF-κB signaling in macrophages: dynamics, crosstalk, and signal integration. Front Immunol 10. https://doi.org/10.3389/fimmu.2019.00705 - PubMed
  44. Draheim T et al (2016) Activation of the astrocytic Nrf2/ARE system ameliorates the formation of demyelinating lesions in a multiple sclerosis animal model. Glia 64:2219–2230. https://doi.org/10.1002/glia.23058 - PubMed
  45. Erny D, Hrabe de Angelis AL, Prinz M (2017) Communicating systems in the body: how microbiota and microglia cooperate. Immunology 150:7–15. https://doi.org/10.1111/imm.12645 - PubMed
  46. Falkowska A, Gutowska I, Goschorska M, Nowacki P, Chlubek D, Baranowska-Bosiacka I (2015) Energy metabolism of the brain, including the cooperation between astrocytes and neurons, especially in the context of glycogen metabolism. Int J Mol Sci 16:25959–25981. https://doi.org/10.3390/ijms161125939 - PubMed
  47. Fazeli PK, Klibanski A (2012) Neuroendocrine dysregulation and the growth hormone-IGF-1 axis in anorexia nervosa. Exp Rev Endocrinol Metab 7:223–231. https://doi.org/10.1586/eem.12.5 - PubMed
  48. Fellin T, Ellenbogen JM, De Pitta M, Ben-Jacob E, Halassa MM (2012) Astrocyte regulation of sleep circuits: experimental and modeling perspectives. Front Comput Neurosci 6:65. https://doi.org/10.3389/fncom.2012.00065 - PubMed
  49. Fetissov SO (2017) Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour. Nat Rev Endocrinol 13:11–25. https://doi.org/10.1038/nrendo.2016.150 - PubMed
  50. Florent V et al (2020) Hypothalamic structural and functional imbalances in anorexia nervosa. Neuroendocrinology 110:552–562. https://doi.org/10.1159/000503147 - PubMed
  51. Fonville L, Giampietro V, Williams SC, Simmons A, Tchanturia K (2014) Alterations in brain structure in adults with anorexia nervosa and the impact of illness duration. Psychol Med 44:1965–1975. https://doi.org/10.1017/s0033291713002389 - PubMed
  52. Frago LM, Chowen JA (2017) Involvement of astrocytes in mediating the central effects of ghrelin. Int J Mol Sci 18.0 https://doi.org/10.3390/ijms18030536 - PubMed
  53. Frintrop L et al (2017) Reduced astrocyte density underlying brain volume reduction in activity-based anorexia rats. World J Biol Psychiatry: 1–11. https://doi.org/10.1080/15622975.2016.1273552 - PubMed
  54. Frintrop L et al (2018) Establishment of a chronic activity-based anorexia rat model. J Neurosci Methods 293:191–198. https://doi.org/10.1016/j.jneumeth.2017.09.018 - PubMed
  55. Frintrop L, Trinh S, Liesbrock J, Leunissen C, Kempermann J, Etdoger S, Kas MJ (2019) The reduction of astrocytes and brain volume loss in anorexia nervosa-the impact of starvation and refeeding in a rodent model. Transl Psychiatry 9:159. https://doi.org/10.1038/s41398-019-0493-7 - PubMed
  56. Fung TC, Olson CA, Hsiao EY (2017) Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 20:145–155. https://doi.org/10.1038/nn.4476 - PubMed
  57. Gianotti L, Lanfranco F, Ramunni J, Destefanis S, Ghigo E, Arvat E (2002) GH/IGF-I axis in anorexia nervosa. Eating Weight Disord 7:94–105. https://doi.org/10.1007/bf03354435 - PubMed
  58. Gibson KR (1991) Brain maturation and cognitive development: comparative and cross-cultural perspectives. Brain maturation and cognitive development: comparative and cross-cultural perspectives. Aldine de Gruyter, Hawthorne - PubMed
  59. Gigante G et al (2011) Role of gut microbiota in food tolerance and allergies. Digest Dis (Basel, Switzerland) 29:540–549. https://doi.org/10.1159/000332977 - PubMed
  60. Godlewska BR, Pike A, Sharpley AL, Ayton A, Park RJ, Cowen PJ, Emir UE (2017) Brain glutamate in anorexia nervosa: a magnetic resonance spectroscopy case control study at 7 Tesla. Psychopharmacology 234:421–426. https://doi.org/10.1007/s00213-016-4477-5 - PubMed
  61. Gonzalez A, Kohn MR, Clarke SD (2007) Eating disorders in adolescents. Aust Fam Physician 36:614–619 - PubMed
  62. Habib P, Dang J, Slowik A, Victor M, Beyer C (2014) Hypoxia-induced gene expression of aquaporin-4, cyclooxygenase-2 and hypoxia-inducible factor 1α in rat cortical astroglia is inhibited by 17β-estradiol and progesterone. Neuroendocrinology 99:156–167. https://doi.org/10.1159/000362279 - PubMed
  63. Hara M, Matsuda Y, Okumura N, Hirai K, Nakagawa H (1989) Effect of glucose starvation on glucose transport in neuronal cells in primary culture from rat brain. J Neurochem 52:909–912. https://doi.org/10.1111/j.1471-4159.1989.tb02541.x - PubMed
  64. Hata T et al (2019) The gut microbiome derived from anorexia nervosa patients impairs weight gain and behavioral performance in female mice. Endocrinology 160:2441–2452. https://doi.org/10.1210/en.2019-00408 - PubMed
  65. Heitzer M, Kaiser S, Kanagaratnam M, Zendedel A, Hartmann P, Beyer C, Johann S (2017) Administration of 17β-estradiol improves Motoneuron survival and Down-regulates Inflammasome activation in male SOD1(G93A) ALS mice. Mol Neurobiol 54:8429–8443. https://doi.org/10.1007/s12035-016-0322-4 - PubMed
  66. Hermens DF, Simcock G, Dutton M, Bouças AP, Can AT, Lilley C, Lagopoulos J (2020) Anorexia nervosa, zinc deficiency and the glutamate system: the ketamine option. Prog Neuro-Psychopharmacol Biol Psychiatry 101:109921. https://doi.org/10.1016/j.pnpbp.2020.109921 - PubMed
  67. Herpertz-Dahlmann B (2015) Adolescent eating disorders: update on definitions, symptomatology, epidemiology, and comorbidity. Child Adolesc Psychiatr Clin N Am 24:177–196. https://doi.org/10.1016/j.chc.2014.08.003 - PubMed
  68. Hoban AE, Stilling RM (2018) The microbiome regulates amygdala-dependent fear recall. Mol Psychiatry 23:1134–1144. https://doi.org/10.1038/mp.2017.100 - PubMed
  69. Holtkamp K, Herpertz-Dahlmann B, Hebebrand K, Mika C, Kratzsch J, Hebebrand J (2006) Physical activity and restlessness correlate with leptin levels in patients with adolescent anorexia nervosa. Biol Psychiatry 60:311–313. https://doi.org/10.1016/j.biopsych.2005.11.001 - PubMed
  70. Hsiao H-Y, Chen Y-C, Chen H-M, Tu P-H, Chern Y (2013) A critical role of astrocyte-mediated nuclear factor-κB-dependent inflammation in Huntington's disease. Hum Mol Genet 22:1826–1842. https://doi.org/10.1093/hmg/ddt036 - PubMed
  71. Huang TT, Lai JB, Du YL, Xu Y, Ruan LM, Hu SH (2019) Current understanding of gut microbiota in mood disorders: an update of human studies. Front Genet 10:98. https://doi.org/10.3389/fgene.2019.00098 - PubMed
  72. Hyvärinen T et al (2019) Co-stimulation with IL-1β and TNF-α induces an inflammatory reactive astrocyte phenotype with neurosupportive characteristics in a human pluripotent stem cell model system. Sci Rep 9:16944. https://doi.org/10.1038/s41598-019-53414-9 - PubMed
  73. Ivanova T, Karolczak M, Beyer C (2002) Estradiol stimulates GDNF expression in developing hypothalamic neurons. Endocrinology 143:3175–3178. https://doi.org/10.1210/endo.143.8.8794 - PubMed
  74. Jiang C, Li G, Huang P, Liu Z, Zhao B (2017) The gut microbiota and Alzheimer’s disease. J Alzheimer’s Dis 58:1–15. https://doi.org/10.3233/jad-161141 - PubMed
  75. Johann S, Beyer C (2013) Neuroprotection by gonadal steroid hormones in acute brain damage requires cooperation with astroglia and microglia. J Steroid Biochem Mol Biol 137:71–81. https://doi.org/10.1016/j.jsbmb.2012.11.006 - PubMed
  76. Joos A et al (2010) Voxel-based morphometry in eating disorders: correlation of psychopathology with grey matter volume. Psychiatry Res 182:146–151. https://doi.org/10.1016/j.pscychresns.2010.02.004 - PubMed
  77. Kaczor P, Rakus D, Mozrzymas JW (2015) Neuron-astrocyte interaction enhance GABAergic synaptic transmission in a manner dependent on key metabolic enzymes. Front Cell Neurosci 9:120. https://doi.org/10.3389/fncel.2015.00120 - PubMed
  78. Kaltschmidt B, Kaltschmidt C (2015) NF-KappaB in long-term memory and structural plasticity in the adult mammalian brain front. Mol Neurosci 8:69–69. https://doi.org/10.3389/fnmol.2015.00069 - PubMed
  79. Kanbur N, Mesci L, Derman O, Turul T, Cuhadaroğlu F, Kutluk T, Tezcan I (2008) Tumor necrosis factor alpha-308 gene polymorphism in patients with anorexia nervosa. Turk J Pediatr 50:219–222 - PubMed
  80. Karki P, Smith K, Johnson J Jr, Lee E (2014) Astrocyte-derived growth factors and estrogen neuroprotection: role of transforming growth factor-α in estrogen-induced upregulation of glutamate transporters in astrocytes. Mol Cell Endocrinol 389:58–64. https://doi.org/10.1016/j.mce.2014.01.010 - PubMed
  81. Kas MJ, Adan RA (2011) Animal models of eating disorder traits. Curr Top Behav Neurosci 6:209–227. https://doi.org/10.1007/7854_2010_84 - PubMed
  82. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science (New York, NY) 305:99–103. https://doi.org/10.1126/science.1096485 - PubMed
  83. Kawai T, Akira S (2007) Signaling to NF-κB by Toll-like receptors. Trends Mol Med 13:460–469. https://doi.org/10.1016/j.molmed.2007.09.002 - PubMed
  84. Kelly JR, Minuto C, Cryan JF, Clarke G, Dinan TG (2017) Cross talk: the microbiota and neurodevelopmental disorders. Front Neurosci 11:490. https://doi.org/10.3389/fnins.2017.00490 - PubMed
  85. Kim JG et al (2014) Leptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding. Nat Neurosci 17:908–910. https://doi.org/10.1038/nn.3725 - PubMed
  86. Kimelberg HK, Nedergaard M (2010) Functions of astrocytes and their potential as therapeutic targets. Neurotherapeutics 7:338–353. https://doi.org/10.1016/j.nurt.2010.07.006 - PubMed
  87. King JA et al (2015) Global cortical thinning in acute anorexia nervosa normalizes following long-term weight restoration. Biol Psychiatry 77:624–632. https://doi.org/10.1016/j.biopsych.2014.09.005 - PubMed
  88. King JA, Frank GKW, Thompson PM, Ehrlich S (2018) Structural neuroimaging of anorexia nervosa: future directions in the quest for mechanisms underlying dynamic alterations. Biol Psychiatry 83:224–234. https://doi.org/10.1016/j.biopsych.2017.08.011 - PubMed
  89. Kipp M, Amor S, Krauth R, Beyer C (2012) Multiple sclerosis: neuroprotective alliance of estrogen-progesterone and gender. Front Neuroendocrinol 33:1–16. https://doi.org/10.1016/j.yfrne.2012.01.001 - PubMed
  90. Kleiman SC, Watson HJ, Bulik-Sullivan EC, Huh EY, Tarantino LM, Bulik CM, Carroll IM (2015) The intestinal microbiota in acute anorexia nervosa and during Renourishment: relationship to depression, anxiety, and eating disorder psychopathology. Psychosom Med 77:969–981. https://doi.org/10.1097/psy.0000000000000247 - PubMed
  91. Klump KL et al (2013) The interactive effects of estrogen and progesterone on changes in emotional eating across the menstrual cycle. J Abnorm Psychol 122:131–137. https://doi.org/10.1037/a0029524 - PubMed
  92. Kogel V, Trinh S, Gasterich N, Beyer C, Seitz J (2021) Long-term glucose starvation induces inflammatory responses and phenotype switch in primary cortical rat astrocytes. J Mol Neurosci. https://doi.org/10.1007/s12031-021-01800-2 - PubMed
  93. Kowiański P, Lietzau G, Czuba E, Waśkow M, Steliga A, Moryś J (2018) BDNF: a key factor with multipotent impact on brain signaling and synaptic plasticity. Cell Mol Neurobiol 38:579–593. https://doi.org/10.1007/s10571-017-0510-4 - PubMed
  94. Lagkouvardos I, Fischer S, Kumar N, Clavel T (2017) Rhea: a transparent and modular R pipeline for microbial profiling based on 16S rRNA gene amplicons. PeerJ 5:e2836. https://doi.org/10.7717/peerj.2836 - PubMed
  95. Landeghem FKHV, Weiss T, Oehmichen M, Deimling AV (2006) Decreased expression of glutamate transporters in astrocytes after human traumatic brain injury. J Neurotrauma 23:1518–1528. https://doi.org/10.1089/neu.2006.23.1518 - PubMed
  96. Lee CY, Dallérac G, Ezan P, Anderova M, Rouach N (2016) Glucose tightly controls morphological and functional properties of astrocytes. Front Aging Neurosci 8:82. https://doi.org/10.3389/fnagi.2016.00082 - PubMed
  97. Levenson JL (2011) The American Psychiatric Publishing textbook of psychosomatic medicine: psychiatric care of the medically ill. American Psychiatric Pub, Washington, DC - PubMed
  98. Li K, Li J, Zheng J, Qin S (2019) Reactive astrocytes in neurodegenerative diseases. Aging Dis 10:664–675. https://doi.org/10.14336/AD.2018.0720 - PubMed
  99. Liddelow SA, Barres BA (2017) Reactive astrocytes: production, function, and therapeutic potential. Immunity 46:957–967. https://doi.org/10.1016/j.immuni.2017.06.006 - PubMed
  100. Liddelow SA et al (2017) Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541:481–487. https://doi.org/10.1038/nature21029 - PubMed
  101. Lim CT, Kola B, Korbonits M (2011) The ghrelin/GOAT/GHS-R system and energy metabolism. Rev Endocr Metab Disord 12:173–186. https://doi.org/10.1007/s11154-011-9169-1 - PubMed
  102. Linnerbauer M, Wheeler MA, Quintana FJ (2020) Astrocyte crosstalk in CNS inflammation. Neuron 108:608–622. https://doi.org/10.1016/j.neuron.2020.08.012 - PubMed
  103. Luz Neto LMD, Vasconcelos FMND, Silva JED, Pinto TCC, Sougey ÉB, Ximenes RCC (2019) Differences in cortisol concentrations in adolescents with eating disorders: a systematic review. J Pediatr 95:18–26. https://doi.org/10.1016/j.jped.2018.02.007 - PubMed
  104. Mack I et al (2016) Weight gain in anorexia nervosa does not ameliorate the faecal microbiota, branched chain fatty acid profiles, and gastrointestinal complaints. Sci Rep 6:26752. https://doi.org/10.1038/srep26752 - PubMed
  105. Mahmoud S, Gharagozloo M, Simard C, Gris D (2019) Astrocytes maintain glutamate homeostasis in the CNS by controlling the balance between glutamate uptake and release. Cell 8. https://doi.org/10.3390/cells8020184 - PubMed
  106. Mainz V, Schulte-Rüther M, Fink GR, Herpertz-Dahlmann B, Konrad K (2012) Structural brain abnormalities in adolescent anorexia nervosa before and after weight recovery and associated hormonal changes. Psychosom Med 74:574–582. https://doi.org/10.1097/PSY.0b013e31824ef10e - PubMed
  107. Mangiola F, Ianiro G, Franceschi F, Fagiuoli S, Gasbarrini G, Gasbarrini A (2016) Gut microbiota in autism and mood disorders. World J Gastroenterol 22:361–368. https://doi.org/10.3748/wjg.v22.i1.361 - PubMed
  108. Margineanu MB et al (2020) Gut microbiota modulates expression of genes involved in the astrocyte-neuron lactate shuttle in the hippocampus. Europ Neuropsychopharmacol 41:152–159. https://doi.org/10.1016/j.euroneuro.2020.11.006 - PubMed
  109. Marina N et al (2018) Brain metabolic sensing and metabolic signaling at the level of an astrocyte. Glia 66:1185–1199. https://doi.org/10.1002/glia.23283 - PubMed
  110. Marques TM, Wall R, Ross RP, Fitzgerald GF, Ryan CA, Stanton C (2010) Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opin Biotechnol 21:149–156. https://doi.org/10.1016/j.copbio.2010.03.020 - PubMed
  111. Martin F (1958) Pathology of the neurological & psychiatric aspects of various manifestations of deficiency diseases with digestive & neuro-endocrine disorders. Praxis 47:197–200 - PubMed
  112. Matejuk A, Ransohoff RM (2020) Crosstalk between astrocytes and microglia: an overview. Front Immunol 11:1416–1416. https://doi.org/10.3389/fimmu.2020.01416 - PubMed
  113. Matsubara M, Sakata I, Wada R, Yamazaki M, Inoue K, Sakai T (2004) Estrogen modulates ghrelin expression in the female rat stomach. Peptides 25:289–297. https://doi.org/10.1016/j.peptides.2003.12.020 - PubMed
  114. Matsumoto M, Kibe R, Ooga T, Aiba Y, Sawaki E, Koga Y, Benno Y (2013) Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study. Front Syst Neurosci 7:9. https://doi.org/10.3389/fnsys.2013.00009 - PubMed
  115. Mattingly D, Bhanji S (1995) Hypoglycaemia and anorexia nervosa. J R Soc Med 88:191–195 - PubMed
  116. Mayorquin LC, Rodriguez AV, Sutachan J-J, Albarracín SL (2018) Connexin-mediated functional and metabolic coupling between astrocytes and neurons. Front Mol Neurosci 11:118–118. https://doi.org/10.3389/fnmol.2018.00118 - PubMed
  117. McCormick LM, Keel PK, Brumm MC, Bowers W, Swayze V, Andersen A, Andreasen N (2008) Implications of starvation-induced change in right dorsal anterior cingulate volume in anorexia nervosa. Int J Eat Disord 41:602–610. https://doi.org/10.1002/eat.20549 - PubMed
  118. Mela V, Vargas A, Meza C, Kachani M, Wagner EJ (2016) Modulatory influences of estradiol and other anorexigenic hormones on metabotropic, Gi/o-coupled receptor function in the hypothalamic control of energy homeostasis. J Steroid Biochem Mol Biol 160:15–26. https://doi.org/10.1016/j.jsbmb.2015.07.014 - PubMed
  119. Mendez P, Wandosell F, Garcia-Segura LM (2006) Cross-talk between estrogen receptors and insulin-like growth factor-I receptor in the brain: cellular and molecular mechanisms. Front Neuroendocrinol 27:391–403. https://doi.org/10.1016/j.yfrne.2006.09.001 - PubMed
  120. Mergenthaler P, Lindauer U, Dienel GA, Meisel A (2013) Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci 36:587–597. https://doi.org/10.1016/j.tins.2013.07.001 - PubMed
  121. Misra M et al (2006) Uncoupling of cardiovascular risk markers in adolescent girls with anorexia nervosa. J Pediatr 149:763–769. https://doi.org/10.1016/j.jpeds.2006.08.043 - PubMed
  122. Mohle L et al (2016) Ly6C(hi) monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep 15:1945–1956. https://doi.org/10.1016/j.celrep.2016.04.074 - PubMed
  123. Molofsky AV et al (2012) Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26:891–907. https://doi.org/10.1101/gad.188326.112 - PubMed
  124. Moresco EM, LaVine D, Beutler B (2011) Toll-like receptors. Curr Biol 21:R488–R493. https://doi.org/10.1016/j.cub.2011.05.039 - PubMed
  125. Morkl S et al (2017) Gut microbiota and body composition in anorexia nervosa inpatients in comparison to athletes, overweight, obese, and normal weight controls. Int J Eat Disord 50:1421–1431. https://doi.org/10.1002/eat.22801 - PubMed
  126. Mortezaee K, Khanlarkhani N, Beyer C, Zendedel A (2018) Inflammasome: its role in traumatic brain and spinal cord injury. J Cell Physiol 233:5160–5169. https://doi.org/10.1002/jcp.26287 - PubMed
  127. Nagl M, Jacobi C, Paul M, Beesdo-Baum K, Höfler M, Lieb R, Wittchen H-U (2016) Prevalence, incidence, and natural course of anorexia and bulimia nervosa among adolescents and young adults. Eur Child Adolesc Psychiatry 25:903–918. https://doi.org/10.1007/s00787-015-0808-z - PubMed
  128. Nagy JI, Rash JE (2000) Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS brain research. Brain Res Rev 32:29–44. https://doi.org/10.1016/s0165-0173(99)00066-1 - PubMed
  129. Nakai Y, Hamagaki S, Takagi R, Taniguchi A, Kurimoto F (2000) Plasma concentrations of tumor necrosis factor-alpha (TNF-alpha) and soluble TNF receptors in patients with bulimia nervosa. Clin Endocrinol 53:383–388. https://doi.org/10.1046/j.1365-2265.2000.01091.x - PubMed
  130. Neufang S, Specht K, Hausmann M, Güntürkün O, Herpertz-Dahlmann B, Fink GR, Konrad K (2009) Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex (New York, NY : 1991) 19:464–473. https://doi.org/10.1093/cercor/bhn100 - PubMed
  131. Neuman H, Debelius JW, Knight R, Koren O (2015) Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev 39:509–521. https://doi.org/10.1093/femsre/fuu010 - PubMed
  132. Neumarker KJ (1997) Mortality and sudden death in anorexia nervosa. Int J Eat Disord 21:205–212 - PubMed
  133. Nobis S et al (2018) Alterations of proteome, mitochondrial dynamic and autophagy in the hypothalamus during activity-based anorexia. Sci Rep 8:7233. https://doi.org/10.1038/s41598-018-25548-9 - PubMed
  134. Noell S, Fallier-Becker P, Beyer C, Kröger S, Mack AF, Wolburg H (2007) Effects of agrin on the expression and distribution of the water channel protein aquaporin-4 and volume regulation in cultured astrocytes. Eur J Neurosci 26:2109–2118. https://doi.org/10.1111/j.1460-9568.2007.05850.x - PubMed
  135. Nogal P, Pniewska-Siark B, Lewinski A (2008) Relation of trophic changes in the central nervous system, measured by the width of cordical sulci, to the clinical course of anorexia nervosa (II). Neuro Endocrinol Lett 29:879–883 - PubMed
  136. Noor SO et al (2010) Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota. BMC Gastroenterol 10:134. https://doi.org/10.1186/1471-230x-10-134 - PubMed
  137. Obata T, Brown GE, Yaffe MB (2000) MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit Care Med 28:N67–N77. https://doi.org/10.1097/00003246-200004001-00008 - PubMed
  138. Ostrowska Z et al (2015) Selected pro-inflammatory cytokines, bone metabolism, osteoprotegerin, and receptor activator of nuclear factor-kB ligand in girls with anorexia nervosa. Endokrynol Pol 66:313–321. https://doi.org/10.5603/ep.2015.0040 - PubMed
  139. Pajarillo E, Rizor A, Lee J, Aschner M, Lee E (2019) The role of astrocytic glutamate transporters GLT-1 and GLAST in neurological disorders: potential targets for neurotherapeutics. Neuropharmacology 161:107559. https://doi.org/10.1016/j.neuropharm.2019.03.002 - PubMed
  140. Panatier A, Robitaille R (2012) Astrocyte, a key partner of neurons during basal synaptic transmission. Med Sci (Paris) 28:582–584. https://doi.org/10.1051/medsci/2012286009 - PubMed
  141. Paulukat L et al (2016) Memory impairment is associated with the loss of regular oestrous cycle and plasma oestradiol levels in an activity-based anorexia animal model. World J Biol Psychiatry 17:274–284. https://doi.org/10.3109/15622975.2016.1173725 - PubMed
  142. Pauwels PJ, Opperdoes FR, Trouet A (1985) Effects of Antimycin, glucose deprivation, and serum on cultures of neurons, astrocytes, and neuroblastoma cells. J Neurochem 44:143–148. https://doi.org/10.1111/j.1471-4159.1985.tb07123.x - PubMed
  143. Pawlak J, Brito V, Küppers E, Beyer C (2005a) Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen brain research. Mol Brain Res 138:1–7. https://doi.org/10.1016/j.molbrainres.2004.10.043 - PubMed
  144. Pawlak J, Karolczak M, Krust A, Chambon P, Beyer C (2005b) Estrogen receptor-alpha is associated with the plasma membrane of astrocytes and coupled to the MAP/Src-kinase pathway. Glia 50:270–275. https://doi.org/10.1002/glia.20162 - PubMed
  145. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91:10625–10629. https://doi.org/10.1073/pnas.91.22.10625 - PubMed
  146. Pellerin L et al (1998) Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 20:291–299. https://doi.org/10.1159/000017324 - PubMed
  147. Pomeroy C, Eckert E, Hu S, Eiken B, Mentink M, Crosby RD, Chao CC (1994) Role of interleukin-6 and transforming growth factor-β in anorexia nervosa. Biol Psychiatry 36:836–839. https://doi.org/10.1016/0006-3223(94)90594-0 - PubMed
  148. Ponath G et al (2016) Myelin phagocytosis by astrocytes after myelin damage promotes lesion pathology. Brain 140:399–413. https://doi.org/10.1093/brain/aww298 - PubMed
  149. Qian Y et al (2007) The adaptor Act1 is required for interleukin 17–dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 8:247–256. https://doi.org/10.1038/ni1439 - PubMed
  150. Queipo-Ortuno MI et al (2013) Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One 8:e65465. https://doi.org/10.1371/journal.pone.0065465 - PubMed
  151. Ragu-Varman D, Macedo-Mendoza M, Labrada-Moncada FE, Reyes-Ortega P, Morales T, Martínez-Torres A, Reyes-Haro D (2019) Anorexia increases microglial density and cytokine expression in the hippocampus of young female rats. Behav Brain Res 363:118–125. https://doi.org/10.1016/j.bbr.2019.01.042 - PubMed
  152. Rahman MH, Kim M-S, Lee I-K, Yu R, Suk K (2018) Interglial crosstalk in obesity-induced hypothalamic inflammation. Front Neurosci 12:939–939. https://doi.org/10.3389/fnins.2018.00939 - PubMed
  153. Ramoz N, Versini A, Gorwood P (2013) Anorexia nervosa and estrogen receptors. Vitam Horm 92:141–163. https://doi.org/10.1016/b978-0-12-410473-0.00006-4 - PubMed
  154. Remely M, Hippe B, Geretschlaeger I, Stegmayer S, Hoefinger I, Haslberger A (2015) Increased gut microbiota diversity and abundance of Faecalibacterium prausnitzii and Akkermansia after fasting: a pilot study. Wien Klin Wochenschr 127:394–398. https://doi.org/10.1007/s00508-015-0755-1 - PubMed
  155. Reyes-Haro D, Labrada-Moncada FE, Miledi R, Martinez-Torres A (2015) Dehydration-induced anorexia reduces astrocyte density in the rat Corpus callosum. Neural Plast 2015:474917. https://doi.org/10.1155/2015/474917 - PubMed
  156. Reyes-Haro D, Labrada-Moncada FE, Varman DR, Kruger J, Morales T, Miledi R, Martinez-Torres A (2016) Anorexia reduces GFAP+ cell density in the rat Hippocampus. Neural Plast 2016:2426413. https://doi.org/10.1155/2016/2426413 - PubMed
  157. Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain-gut-enteric microbiota axis Nature reviews. Gastroenterol Hepatol 6:306–314. https://doi.org/10.1038/nrgastro.2009.35 - PubMed
  158. Ribasés M et al (2003) Met66 in the brain-derived neurotrophic factor (BDNF) precursor is associated with anorexia nervosa restrictive type. Mol Psychiatry 8:745–751. https://doi.org/10.1038/sj.mp.4001281 - PubMed
  159. Ridaura VK et al. (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science (New York, NY) 341:1241214. https://doi.org/10.1126/science.1241214 - PubMed
  160. Rothhammer V, Mascanfroni ID, Bunse L (2016) Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat Med 22:586–597. https://doi.org/10.1038/nm.4106 - PubMed
  161. Routtenberg A, Kuznesof AW (1967) Self-starvation of rats living in activity wheels on a restricted feeding schedule. J Comp Physiol Psychol 64:414–421 - PubMed
  162. Schattner A, Tepper R, Steinbock M, Hahn T, Schoenfeld A (1990) TNF, interferon-gamma and cell-mediated cytotoxicity in anorexia nervosa; effect of refeeding. J Clin Lab Immunol 32:183–184 - PubMed
  163. Schattner A, Tepper R, Steinbock M, Schoenfeld A, Vaisman N, Hahn T (1992) Cytokines in anorexia nervosa–nutritional or neuroimmunal changes? Harefuah 123:245–247. 308 - PubMed
  164. Scheld M et al (2016) Neurodegeneration triggers peripheral immune cell recruitment into the forebrain. J Neurosci 36:1410–1415. https://doi.org/10.1523/jneurosci.2456-15.2016 - PubMed
  165. Schorr M, Miller KK (2017) The endocrine manifestations of anorexia nervosa: mechanisms and management. Nat Rev Endocrinol 13:174–186. https://doi.org/10.1038/nrendo.2016.175 - PubMed
  166. Seitz J, Walter M, Mainz V, Herpertz-Dahlmann B, Konrad K, von Polier G (2015) Brain volume reduction predicts weight development in adolescent patients with anorexia nervosa. J Psychiatr Res 68:228–237. https://doi.org/10.1016/j.jpsychires.2015.06.019 - PubMed
  167. Seitz J, Herpertz-Dahlmann B, Konrad K (2016) Brain morphological changes in adolescent and adult patients with anorexia nervosa. J Neural Trans (Vienna, Austria : 1996) 123:949–959. https://doi.org/10.1007/s00702-016-1567-9 - PubMed
  168. Seitz J, Konrad K, Herpertz-Dahlmann B (2018) Extend, Pathomechanism and clinical consequences of brain volume changes in anorexia nervosa. Curr Neuropharmacol 16:1164–1173. https://doi.org/10.2174/1570159x15666171109145651 - PubMed
  169. Seitz J, Trinh S, Herpertz-Dahlmann B (2019) The microbiome and eating disorders. Psychiatr Clin North Am 42:93–103. https://doi.org/10.1016/j.psc.2018.10.004 - PubMed
  170. Sender R, Fuchs S (2016) Revised estimates for the number of human and Bacteria cells in the body. PLoS Biol 14:e1002533. https://doi.org/10.1371/journal.pbio.1002533 - PubMed
  171. Seong J, Kang JY, Sun JS, Kim KW (2019) Hypothalamic inflammation and obesity: a mechanistic review. Arch Pharm Res 42:383–392. https://doi.org/10.1007/s12272-019-01138-9 - PubMed
  172. Sgritta M, Dooling SW, Buffington SA, Momin EN, Francis MB, Britton RA, Costa-Mattioli M (2019) Mechanisms underlying microbial-mediated changes in social behavior in mouse models of Autism Spectrum Disorder. Neuron 101:246–259.e246. https://doi.org/10.1016/j.neuron.2018.11.018 - PubMed
  173. Shaw P et al (2008) Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28:3586–3594. https://doi.org/10.1523/jneurosci.5309-07.2008 - PubMed
  174. Sidoryk-Wegrzynowicz M, Wegrzynowicz M, Lee E, Bowman AB, Aschner M (2011) Role of astrocytes in brain function and disease. Toxicol Pathol 39:115–123. https://doi.org/10.1177/0192623310385254 - PubMed
  175. Simon LS (1999) Role and regulation of cyclooxygenase-2 during inflammation. Am J Med 106:37s–42s. https://doi.org/10.1016/s0002-9343(99)00115-1 - PubMed
  176. Singhal V, Misra M, Klibanski A (2014) Endocrinology of anorexia nervosa in young people: recent insights. Curr Opin Endocrinol Diabetes Obes 21:64–70. https://doi.org/10.1097/med.0000000000000026 - PubMed
  177. Slowik A, Lammerding L, Hoffmann S, Beyer C (2018) Brain inflammasomes in stroke and depressive disorders: regulation by oestrogen. J Neuroendocrinol 30. https://doi.org/10.1111/jne.12482 - PubMed
  178. Smink FR, van Hoeken D, Hoek HW (2012) Epidemiology of eating disorders: incidence, prevalence and mortality rates. Curr Psychiatry Rep 14:406–414. https://doi.org/10.1007/s11920-012-0282-y - PubMed
  179. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638–647. https://doi.org/10.1016/j.tins.2009.08.002 - PubMed
  180. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7–35. https://doi.org/10.1007/s00401-009-0619-8 - PubMed
  181. Sohrabji F, Lewis DK (2006) Estrogen-BDNF interactions: implications for neurodegenerative diseases. Front Neuroendocrinol 27:404–414. https://doi.org/10.1016/j.yfrne.2006.09.003 - PubMed
  182. Solmi M, Veronese N, Favaro A, Santonastaso P, Manzato E, Sergi G, Correll CU (2015) Inflammatory cytokines and anorexia nervosa: a meta-analysis of cross-sectional and longitudinal studies. Psychoneuroendocrinology 51:237–252. https://doi.org/10.1016/j.psyneuen.2014.09.031 - PubMed
  183. Sonoyama K, Fujiwara R, Takemura N, Ogasawara T, Watanabe J, Ito H, Morita T (2009) Response of gut microbiota to fasting and hibernation in Syrian hamsters. Appl Environ Microbiol 75:6451–6456. https://doi.org/10.1128/aem.00692-09 - PubMed
  184. Steinhausen HC, Jensen CM (2015) Time trends in lifetime incidence rates of first-time diagnosed anorexia nervosa and bulimia nervosa across 16 years in a Danish nationwide psychiatric registry study. Int J Eat Disord 48:845–850. https://doi.org/10.1002/eat.22402 - PubMed
  185. Støving RK, Hangaard J, Hansen-Nord M, Hagen C (1999) A review of endocrine changes in anorexia nervosa. J Psychiatr Res 33:139–152. https://doi.org/10.1016/s0022-3956(98)00049-1 - PubMed
  186. Subramanian S, Campbell BJ, Rhodes JM (2006) Bacteria in the pathogenesis of inflammatory bowel disease. Curr Opin Infect Dis 19:475–484. https://doi.org/10.1097/01.qco.0000244054.69253.f3 - PubMed
  187. Sun D, Jakobs TC (2012) Structural remodeling of astrocytes in the injured CNS. Neuroscientist 18:567–588. https://doi.org/10.1177/1073858411423441 - PubMed
  188. Ticinesi A, Lauretani F, Tana C, Nouvenne A, Ridolo E, Meschi T (2019) Exercise and immune system as modulators of intestinal microbiome: implications for the gut-muscle axis hypothesis. Exerc Immunol Rev 25:84–95 - PubMed
  189. Treasure J, Willmott D (2020) Cognitive interpersonal model for anorexia nervosa revisited: the perpetuating factors that contribute to the development of the severe and enduring illness. J Clin Med 9. https://doi.org/10.3390/jcm9030630 - PubMed
  190. Treasure J, Stein D, Maguire S (2015) Has the time come for a staging model to map the course of eating disorders from high risk to severe enduring illness? An examination of the evidence. Early Interv Psychiatry 9:173–184. https://doi.org/10.1111/eip.12170 - PubMed
  191. Trinh S et al (2021) Gut microbiota and brain alterations in a translational anorexia nervosa rat model. J Psychiatr Res 133:156–165. https://doi.org/10.1016/j.jpsychires.2020.12.030 - PubMed
  192. Victor VM et al (2014) Altered mitochondrial function and oxidative stress in leukocytes of anorexia nervosa patients. PLoS One 9:e106463. https://doi.org/10.1371/journal.pone.0106463 - PubMed
  193. Vogel K et al (2016) White matter microstructural changes in adolescent anorexia nervosa including an exploratory longitudinal study. Neuroimage Clin 11:614–621. https://doi.org/10.1016/j.nicl.2016.04.002 - PubMed
  194. Wang P, Liu C, Liu L, Zhang X, Ren B, Li B (2015) The antidepressant-like effects of estrogen-mediated ghrelin. Curr Neuropharmacol 13:524–535. https://doi.org/10.2174/1570159x1304150831120650 - PubMed
  195. Yang Z, Wang KKW (2015) Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci 38:364–374. https://doi.org/10.1016/j.tins.2015.04.003 - PubMed
  196. Yang J et al (2017) The multiple roles of XBP1 in regulation of glucose and lipid metabolism. Curr Protein Pept Sci 18:630–635. https://doi.org/10.2174/1389203717666160627085011 - PubMed
  197. Young JK (2010) Anorexia nervosa and estrogen: current status of the hypothesis. Neurosci Biobehav Rev 34:1195–1200. https://doi.org/10.1016/j.neubiorev.2010.01.015 - PubMed
  198. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, Barres BA (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32:6391–6410. https://doi.org/10.1523/JNEUROSCI.6221-11.2012 - PubMed
  199. Zelante T et al (2013) Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372–385. https://doi.org/10.1016/j.immuni.2013.08.003 - PubMed
  200. Zou J et al (2019) Mechanisms shaping the role of ERK1/2 in cellular senescence (review). Mol Med Rep 19:759–770. https://doi.org/10.3892/mmr.2018.9712 - PubMed

Publication Types