The interoceptive hippocampus: Mouse brain endocrine receptor expression highlights a dentate gyrus (DG)–cornu ammonis (CA) challenge–sufficiency axis

English version

Autoři: Richard Lathe ^aff001; Sheena Singadia ^aff002; Crispin Jordan ^aff003; Gernot Riedel ^aff002
Působiště autorů: Division of Infection Medicine, University of Edinburgh Medical School, Little France, Edinburgh, Scotland, United Kingdom ^aff001; Division of Behavioral Neuroscience, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, Scotland, United Kingdom ^aff002; Division of Biomedical Sciences, University of Edinburgh Medical School, George Square, Edinburgh, Scotland, United Kingdom ^aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227575

Souhrn

The primeval function of the mammalian hippocampus (HPC) remains uncertain. Implicated in learning and memory, spatial navigation, and neuropsychological disorders, evolutionary theory suggests that the HPC evolved from a primeval chemosensory epithelium. Deficits in sensing of internal body status ('interoception') in patients with HPC lesions argue that internal sensing may be conserved in higher vertebrates. We studied the expression patterns in mouse brain of 250 endocrine receptors that respond to blood-borne ligands. Key findings are (i) the proportions and levels of endocrine receptor expression in the HPC are significantly higher than in all other comparable brain regions. (ii) Surprisingly, the distribution of endocrine receptor expression within mouse HPC was found to be highly structured: receptors signaling 'challenge' are segregated in dentate gyrus (DG), whereas those signaling 'sufficiency' are principally found in cornu ammonis (CA) regions. Selective expression of endocrine receptors in the HPC argues that interoception remains a core feature of hippocampal function. Further, we report that ligands of DG receptors predominantly inhibit both synaptic potentiation and neurogenesis, whereas CA receptor ligands conversely promote both synaptic potentiation and neurogenesis. These findings suggest that the hippocampus acts as an integrator of body status, extending its role in context-dependent memory encoding from 'where' and 'when' to 'how I feel'. Implications for anxiety and depression are discussed.

Klíčová slova:

Cytokines – Endocrine physiology – Fibroblast growth factor – Gene expression – Hippocampal neurogenesis – Hippocampus – Neurogenesis – Receptor physiology

Zdroje

1. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci. 2002;3, 655–666. doi: 10.1038/nrn894 12154366

2. Scoville WB and Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiat. 1957;20, 11–21. doi: 10.1136/jnnp.20.1.11 13406589

3. Hebben N, Corkin S, Eichenbaum H, Shedlack K. Diminished ability to interpret and report internal states after bilateral medial temporal resection: case H.M. Behav Neurosci. 1985;99, 1031–1039. doi: 10.1037//0735-7044.99.6.1031 3843537

4. Davidson TL and Jarrard LE. A role for hippocampus in the utilization of hunger signals. Behav Neural Biol. 1993;59, 167–171. doi: 10.1016/0163-1047(93)90925-8 8476385

5. Clifton PG, Vickers SP, Somerville EM. Little and often: ingestive behaviour patterns following hippocampal lesions in rats. Behav Neurosci. 1998;112, 502–511. doi: 10.1037//0735-7044.112.3.502 9676968

6. Davidson TL, Kanoski SE, Chan K, Clegg DJ, Benoit SC, Jarrard LE. Hippocampal lesions impair retention of discriminative responding based on energy state cues. Behav Neurosci. 2010;124, 97–105. doi: 10.1037/a0018402 20141284

7. Riss W, Halpern M, Scalia F. Anatomical aspects of the evolution of the limbic and olfactory systems and their potential significance for behaviour. Ann NY Acad Sci. 1969;159, 1096–1111. doi: 10.1111/j.1749-6632.1969.tb13000.x 5260291

8. Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C. The Central Nervous System of Vertebrates. Berlin: Springer; 1997.

9. Lathe R. Hormones and the hippocampus. J Endocrinol. 2001;169, 205–231. doi: 10.1677/joe.0.1690205 11312139

10. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol. 1969;137, 433–457. doi: 10.1002/cne.901370404 5361244

11. Lledo PM and Valley M. Adult olfactory bulb neurogenesis. Cold Spring Harb Perspect Biol. 2016;8.

12. Wilken MS and Reh TA. Retinal regeneration in birds and mice. Curr Opin Genet Dev. 2016;40, 57–64. doi: 10.1016/j.gde.2016.05.028 27379897

13. Ming GL and Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 2011;70, 687–702. doi: 10.1016/j.neuron.2011.05.001 21609825

14. Duvernoy H, Cattin F, Risold P-Y. The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI. Heidelberg: Springer; 2013.

15. Lein ES, Zhao X, Gage FH. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci. 2004;24, 3879–3889. doi: 10.1523/JNEUROSCI.4710-03.2004 15084669

16. Bienkowski MS, Bowman I, Song MY, Gou L, Ard T, Cotter K et al. Integration of gene expression and brain-wide connectivity reveals the multiscale organization of mouse hippocampal networks. Nat Neurosci. 2018;21, 1628–1643. doi: 10.1038/s41593-018-0241-y 30297807

17. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT et al. Genomic anatomy of the hippocampus. Neuron. 2008;60, 1010–1021. doi: 10.1016/j.neuron.2008.12.008 19109908

18. Thompson CL, Ng L, Menon V, Martinez S, Lee CK, Glattfelder K et al. A high-resolution spatiotemporal atlas of gene expression of the developing mouse brain. Neuron. 2014;83, 309–323. doi: 10.1016/j.neuron.2014.05.033 24952961

19. Stapleton G, Steel M, Richardson M, Mason JO, Rose KA, Morris RG et al. A novel cytochrome P450 expressed primarily in brain. J Biol Chem. 1995;270, 29739–29745. doi: 10.1074/jbc.270.50.29739 8530364

20. Davies BJ, Pickard BS, Steel M, Morris RG, Lathe R. Serine proteases in rodent hippocampus. J Biol Chem. 1998;273, 23004–22011. doi: 10.1074/jbc.273.36.23004 9722524

21. Steel M, Moss J, Clark KA, Kearns IR, Davies CH, Morris RG et al. Gene-trapping to identify and analyze genes expressed in the mouse hippocampus. Hippocampus. 1998;8, 444–457. doi: 10.1002/(SICI)1098-1063(1998)8:5<444::AID-HIPO5>3.0.CO;2-X 9825957

22. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature. 2007;445, 168–176. doi: 10.1038/nature05453 17151600

23. Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics. 2017;18, 529. doi: 10.1186/s12859-017-1934-z 29187165

24. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9, 671–675. doi: 10.1038/nmeth.2089 22930834

25. R Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2019.

26. Canty A and Ripley B. Boot: bootstrap R (S-Plus) functions. R package version 1 3–20. 2017.

27. Davison AC and Hinkley DV. Bootstrap Methods and Their Applications. Cambridge: Cambridge University Press; 1997.

28. Cembrowski MS, Wang L, Sugino K, Shields BC, Spruston N. Hipposeq: a comprehensive RNA-seq database of gene expression in hippocampal principal neurons. Elife. 2016;5, e14997. doi: 10.7554/eLife.14997 27113915

29. Tancredi V, Zona C, Velotti F, Eusebi F, Santoni A. Interleukin-2 suppresses established long-term potentiation and inhibits its induction in the rat hippocampus. Brain Res. 1990;525, 149–151. doi: 10.1016/0006-8993(90)91331-a 2173960

30. Katsuki H, Nakai S, Hirai Y, Akaji K, Kiso Y, Satoh M. Interleukin-1 beta inhibits long-term potentiation in the CA3 region of mouse hippocampal slices. Eur J Pharmacol. 1990;181, 323–326. doi: 10.1016/0014-2999(90)90099-r 2166677

31. Tancredi V, D'Arcangelo G, Grassi F, Tarroni P, Palmieri G, Santoni A et al. Tumor necrosis factor alters synaptic transmission in rat hippocampal slices. Neurosci Lett. 1992;146, 176–178. doi: 10.1016/0304-3940(92)90071-e 1337194

32. Bellinger FP, Madamba S, Siggins GR. Interleukin 1 beta inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Res. 1993;628, 227–234. doi: 10.1016/0006-8993(93)90959-q 8313151

33. Coogan A and O'Connor JJ. Inhibition of NMDA receptor-mediated synaptic transmission in the rat dentate gyrus in vitro by IL-1 beta. Neuroreport. 1997;8, 2107–2110. doi: 10.1097/00001756-199707070-00004 9243593

34. Ikegaya Y, Saito H, Torii K, Nishiyama N. Activin selectively abolishes hippocampal long-term potentiation induced by weak tetanic stimulation in vivo. Jpn J Pharmacol. 1997;75, 87–89. doi: 10.1254/jjp.75.87 9334889

35. Mendoza-Fernandez V, Andrew RD, Barajas-Lopez C. Interferon-alpha inhibits long-term potentiation and unmasks a long-term depression in the rat hippocampus. Brain Res. 2000;885, 14–24. doi: 10.1016/s0006-8993(00)02877-8 11121525

36. Griffin R, Nally R, Nolan Y, McCartney Y, Linden J, Lynch MA. The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem. 2006;99, 1263–1272. doi: 10.1111/j.1471-4159.2006.04165.x 16981890

37. Ishiyama J, Saito H, Abe K. Epidermal growth factor and basic fibroblast growth factor promote the generation of long-term potentiation in the dentate gyrus of anaesthetized rats. Neurosci Res. 1991;12, 403–411. doi: 10.1016/0168-0102(91)90071-6 1664922

38. Matsuoka N, Kaneko S, Satoh M. Somatostatin augments long-term potentiation of the mossy fiber-CA3 system in guinea-pig hippocampal slices. Brain Res. 1991;553, 188–194. doi: 10.1016/0006-8993(91)90823-e 1681981

39. Hisajima H, Saito H, Abe K, Nishiyama N. Effects of acidic fibroblast growth factor on hippocampal long-term potentiation in fasted rats. J Neurosci Res. 1992;31, 549–553. doi: 10.1002/jnr.490310319 1379306

40. Yasui M and Kawasaki K. CCKB-receptor activation augments the long-term potentiation in guinea pig hippocampal slices. Jpn J Pharmacol. 1995;68, 441–447. doi: 10.1254/jjp.68.441 8531419

41. Vara H, Munoz-Cuevas J, Colino A. Age-dependent alterations of long-term synaptic plasticity in thyroid-deficient rats. Hippocampus. 2003;13, 816–825. doi: 10.1002/hipo.10132 14620877

42. Dong J, Yin H, Liu W, Wang P, Jiang Y, Chen J. Congenital iodine deficiency and hypothyroidism impair LTP and decrease C-fos and C-jun expression in rat hippocampus. Neurotoxicology. 2005;26, 417–426. doi: 10.1016/j.neuro.2005.03.003 15935212

43. Taskin E, Artis AS, Bitiktas S, Dolu N, Liman N, Suer C. Experimentally induced hyperthyroidism disrupts hippocampal long-term potentiation in adult rats. Neuroendocrinology. 2011;94, 218–227. doi: 10.1159/000328513 21778690

44. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z et al. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci. 2006;26, 9703–9712. doi: 10.1523/JNEUROSCI.2723-06.2006 16988041

45. Erta M, Quintana A, Hidalgo J. Interleukin-6, a major cytokine in the central nervous system. Int J Biol Sci. 2012;8, 1254–1266. doi: 10.7150/ijbs.4679 23136554

46. Vallieres L, Campbell IL, Gage FH, Sawchenko PE. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci. 2002;22, 486–492. doi: 10.1523/JNEUROSCI.22-02-00486.2002 11784794

47. Saaltink DJ and Vreugdenhil E. Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition? Cell Mol Life Sci. 2014;71, 2499–2515. doi: 10.1007/s00018-014-1568-5 24522255

48. Odaka H, Adachi N, Numakawa T. Impact of glucocorticoid on neurogenesis. Neural Regen Res. 2017;12, 1028–1035. doi: 10.4103/1673-5374.211174 28852377

49. Borsini A, Alboni S, Horowitz MA, Tojo LM, Cannazza G, Su KP et al. Rescue of IL-1beta-induced reduction of human neurogenesis by omega-3 fatty acids and antidepressants. Brain Behav Immun. 2017;65, 230–238. doi: 10.1016/j.bbi.2017.05.006 28529072

50. Borsini A, Cattaneo A, Malpighi C, Thuret S, Harrison NA, Zunszain PA et al. Interferon-alpha reduces human hippocampal neurogenesis and increases apoptosis via activation of distinct STAT1-dependent mechanisms. Int J Neuropsychopharmacol. 2018;21, 187–200. doi: 10.1093/ijnp/pyx083 29040650

51. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C et al. FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci U S A. 2001;98, 5874–5879. doi: 10.1073/pnas.101034998 11320217

52. Fowler CD, Liu Y, Wang Z. Estrogen and adult neurogenesis in the amygdala and hypothalamus. Brain Res Rev. 2008;57, 342–351. doi: 10.1016/j.brainresrev.2007.06.011 17764748

53. Suzuki S, Gerhold LM, Bottner M, Rau SW, Dela CC, Yang E et al. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol. 2007;500, 1064–1075. doi: 10.1002/cne.21240 17183542

54. Chan M, Chow C, Hamson DK, Lieblich SE, Galea LA. Effects of chronic oestradiol, progesterone and medroxyprogesterone acetate on hippocampal neurogenesis and adrenal mass in adult female rats. J Neuroendocrinol. 2014;26, 386–399. doi: 10.1111/jne.12159 24750490

55. Kang W and Hebert JM. FGF signaling is necessary for neurogenesis in young mice and sufficient to reverse its decline in old mice. J Neurosci. 2015;35, 10217–10223. doi: 10.1523/JNEUROSCI.1469-15.2015 26180198

56. Bingman VP and Muzio RN. Reflections on the structural-functional evolution of the hippocampus: what is the big deal about a dentate gyrus? Brain Behav Evol. 2017;90, 53–61. doi: 10.1159/000475592 28866681

57. Gray JA. The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-Hippocampal System. Oxford: Oxford University Press; 1982.

58. Gray JA and McNaughton N. The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-Hippocampal System. Oxford: Oxford University Press; 2000.

59. Smith JW, Urba WJ, Curti BD, Elwood LJ, Steis RG, Janik JE et al. The toxic and hematologic effects of interleukin-1 alpha administered in a phase I trial to patients with advanced malignancies. J Clin Oncol. 1992;10, 1141–1152. doi: 10.1200/JCO.1992.10.7.1141 1607919

60. Capuron L, Ravaud A, Gualde N, Bosmans E, Dantzer R, Maes M et al. Association between immune activation and early depressive symptoms in cancer patients treated with interleukin-2-based therapy. Psychoneuroendocrinology. 2001;26, 797–808. doi: 10.1016/s0306-4530(01)00030-0 11585680

61. Valentine AD, Meyers CA, Kling MA, Richelson E, Hauser P. Mood and cognitive side effects of interferon-alpha therapy. Semin Oncol. 1998;25, 39–47.

62. Raison CL, Demetrashvili M, Capuron L, Miller AH. Neuropsychiatric adverse effects of interferon-alpha: recognition and management. CNS Drugs. 2005;19, 105–123. doi: 10.2165/00023210-200519020-00002 15697325

63. Exton MS, Baase J, Pithan V, Goebel MU, Limmroth V, Schedlowski M. Neuropsychological performance and mood states following acute interferon-beta-1b administration in healthy males. Neuropsychobiology. 2002;45, 199–204. doi: 10.1159/000063671 12097809

64. Creaven PJ, Plager JE, Dupere S, Huben RP, Takita H, Mittelman A et al. Phase I clinical trial of recombinant human tumor necrosis factor. Cancer Chemother Pharmacol. 1987;20, 137–144. doi: 10.1007/bf00253968 3664933

65. Zarrouf FA, Artz S, Griffith J, Sirbu C, Kommor M. Testosterone and depression: systematic review and meta-analysis. J Psychiatr Pract. 2009;15, 289–305. doi: 10.1097/01.pra.0000358315.88931.fc 19625884

66. Gruber AJ and Pope HG Jr. Psychiatric and medical effects of anabolic-androgenic steroid use in women. Psychother Psychosom. 2000;69, 19–26. doi: 10.1159/000012362 10601831

67. Bauer M, Hellweg R, Graf KJ, Baumgartner A. Treatment of refractory depression with high-dose thyroxine. Neuropsychopharmacology. 1998;18, 444–455. doi: 10.1016/S0893-133X(97)00181-4 9571653

68. Hanson ND, Owens MJ, Nemeroff CB. Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology. 2011;36, 2589–2602. doi: 10.1038/npp.2011.220 21937982

69. Yan HC, Cao X, Gao TM, Zhu XH. Promoting adult hippocampal neurogenesis: a novel strategy for antidepressant drug screening. Curr Med Chem. 2011;18, 4359–4367. doi: 10.2174/092986711797200471 21861813

70. Weiland NG, Orikasa C, Hayashi S, McEwen BS. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol. 1997;388, 603–612. doi: 10.1002/(sici)1096-9861(19971201)388:4<603::aid-cne8>3.0.co;2-6 9388019

71. Walf AA and Frye CA. A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology. 2006;31, 1097–1111. doi: 10.1038/sj.npp.1301067 16554740

72. Bean LA, Ianov L, Foster TC. Estrogen receptors, the hippocampus, and memory. Neuroscientist. 2014;20, 534–545. doi: 10.1177/1073858413519865 24510074

73. Sugiyama N, Andersson S, Lathe R, Fan X, Alonso-Magdalena P, Schwend T et al. Spatiotemporal dynamics of the expression of estrogen receptors in the postnatal mouse brain. Mol Psychiatry. 2009;14, 223–32, 117. doi: 10.1038/mp.2008.118 18982005

74. Wei W, Schwaid AG, Wang X, Wang X, Chen S, Chu Q et al. Ligand activation of ERRalpha by cholesterol mediates statin and bisphosphonate effects. Cell Metab. 2016;23, 479–491. doi: 10.1016/j.cmet.2015.12.010 26777690

75. Shughrue PJ and Merchenthaler I. Evidence for novel estrogen binding sites in the rat hippocampus. Neuroscience. 2000;99, 605–612. doi: 10.1016/s0306-4522(00)00242-6 10974424

76. Thin TH, Kim E, Yeh S, Sampson ER, Chen YT, Collins LL et al. Mutations in the helix 3 region of the androgen receptor abrogate ARA70 promotion of 17beta-estradiol-induced androgen receptor transactivation. J Biol Chem. 2002;277, 36499–36508. doi: 10.1074/jbc.M202824200 12068007

77. Bjerregaard-Olesen C, Ghisari M, Kjeldsen LS, Wielsoe M, Bonefeld-Jorgensen EC. Estrone sulfate and dehydroepiandrosterone sulfate: transactivation of the estrogen and androgen receptor. Steroids. 2016;105, 50–58. doi: 10.1016/j.steroids.2015.11.009 26666359

78. Lathe R and Kotelevtsev Y. Steroid signaling: ligand-binding promiscuity, molecular symmetry, and the need for gating. Steroids. 2014;82, 14–22. doi: 10.1016/j.steroids.2014.01.002 24462647

79. Rose K, Allan A, Gauldie S, Stapleton G, Dobbie L, Dott K et al. Neurosteroid hydroxylase CYP7B: vivid reporter activity in dentate gyrus of gene-targeted mice and abolition of a widespread pathway of steroid and oxysterol hydroxylation. J Biol Chem. 2001;276, 23937–23944. doi: 10.1074/jbc.M011564200 11290741

80. Beenken A and Mohammadi M. The structural biology of the FGF19 subfamily. Adv Exp Med Biol. 2012;728, 1–24. doi: 10.1007/978-1-4614-0887-1_1 22396159

81. Itoh N, Ohta H, Konishi M. Endocrine FGFs: evolution, physiology, pathophysiology, and pharmacotherapy. Front Endocrinol 2015;6, 154.

82. Jost B, Duluc I, Richardson M, Lathe R, Freund JN. Functional diversity and interactions between the repeat domains of rat intestinal lactase. Biochem J. 1997;327, 95–103. doi: 10.1042/bj3270095 9355740

83. Fon TK, Bookout AL, Ding X, Kurosu H, John GB, Wang L et al. Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol. 2010;24, 2050–2064. doi: 10.1210/me.2010-0142 20667984

84. Eigler T and Ben-Shlomo A. Somatostatin system: molecular mechanisms regulating anterior pituitary hormones. J Mol Endocrinol. 2014;53, R1–19. doi: 10.1530/JME-14-0034 24780840

85. Prévot TD, Gastambide F, Viollet C, Henkous N, Martel G, Epelbaum J et al. Roles of hippocampal somatostatin receptor subtypes in stress response and emotionality. Neuropsychopharmacology. 2017;42, 1647–1656. doi: 10.1038/npp.2016.281 27986975

86. Gastambide F, Viollet C, Lepousez G, Epelbaum J, Guillou JL. Hippocampal SSTR4 somatostatin receptors control the selection of memory strategies. Psychopharmacology (Berl). 2009;202, 153–163.

87. Gastambide F, Lepousez G, Viollet C, Loudes C, Epelbaum J, Guillou JL. Cooperation between hippocampal somatostatin receptor subtypes 4 and 2: functional relevance in interactive memory systems. Hippocampus. 2010;20, 745–757. doi: 10.1002/hipo.20680 19623609

88. Prévot TD, Viollet C, Epelbaum J, Dominguez G, Beracochea D, Guillou JL. Sst2-receptor gene deletion exacerbates chronic stress-induced deficits: consequences for emotional and cognitive ageing. Prog Neuropsychopharmacol Biol Psychiatry. 2018;86, 390–400. doi: 10.1016/j.pnpbp.2018.01.022 29409919

89. Chapman K, Holmes M, Seckl J. 11beta-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol Rev. 2013;93, 1139–1206. doi: 10.1152/physrev.00020.2012 23899562

90. De Kloet ER, Reul JM, Sutanto W. Corticosteroids and the brain. J Steroid Biochem Mol Biol. 1990;37, 387–394. doi: 10.1016/0960-0760(90)90489-8 2257242

91. Pryce CR, Feldon J, Fuchs E, Knuesel I, Oertle T, Sengstag C et al. Postnatal ontogeny of hippocampal expression of the mineralocorticoid and glucocorticoid receptors in the common marmoset monkey. Eur J Neurosci. 2005;21, 1521–1535. doi: 10.1111/j.1460-9568.2005.04003.x 15845080

92. Seckl JR, Dickson KL, Yates C, Fink G. Distribution of glucocorticoid and mineralocorticoid receptor messenger RNA expression in human postmortem hippocampus. Brain Res. 1991;561, 332–337. doi: 10.1016/0006-8993(91)91612-5 1666329

93. Huang C, Wan B, Gao B, Hexige S, Yu L. Isolation and characterization of novel human short-chain dehydrogenase/reductase SCDR10B which is highly expressed in the brain and acts as hydroxysteroid dehydrogenase. Acta Biochim Pol. 2009;56, 279–289. 19436836

The interoceptive hippocampus: Mouse brain endocrine receptor expression highlights a dentate gyrus (DG)–cornu ammonis (CA) challenge–sufficiency axis

Souhrn

Klíčová slova:

Zdroje

PLOS One

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