Satb2 Ablation Impairs Hippocampus-Based Long-Term Spatial Memory and Short-Term Working Memory and Immediate Early Genes (IEGs)-Mediated Hippocampal Synaptic Plasticity

  • Ying Li
  • Qiang-Long You
  • Sheng-Rong Zhang
  • Wei-Yuan Huang
  • Wen-Jun Zou
  • Wei Jie
  • Shu-Ji Li
  • Ji-Hong Liu
  • Chuang-Ye Lv
  • Jin Cong
  • Yu-Ying Hu
  • Tian-Ming GaoEmail author
  • Jian-Ming LiEmail author


Special AT-rich sequence-binding protein 2 (Satb2) is a protein binding to the matrix attachment regions of DNA and important for gene regulation. Patients with SATB2 mutation usually suffer moderate to severe mental retardation. However, the mechanisms for the defects of intellectual activities in patients with SATB2 mutation are largely unclear. Here we established the heterozygous Satb2 mutant mice and Satb2 conditional knockout mice to mimic the patients with SATB2 mutation and figured out the role of Satb2 in mental activities. We found that the spatial memory and working memory were significantly damaged in the heterozygous Satb2 mutant mice, early postnatal Satb2-deficient mice (CaMKIIα-Cre+Satb2fl/fl mice), and adult Satb2 ablation mice (Satb2fl/fl mice injected with CaMKIIα-Cre virus). Functionally, late phase long-term potentiation (L-LTP) in these Satb2 mutant mice was greatly impaired. Morphologically, in CA1 neurons of CaMKIIα-Cre+Satb2fl/fl mice, we found decreased spine density of the basal dendrites and less branches of apical dendrites that extended into lacunar molecular layer. Mechanistically, expression levels of immediate early genes (IEGs) including Fos, FosB, and Egr1 were significantly decreased after Satb2 deletion. And, Satb2 could regulate expression of FosB by binding to the promoter of FosB directly. In general, our study uncovers that Satb2 plays an important role in spatial memory and working memory by regulating IEGs-mediated hippocampal synaptic plasticity.


Satb2 Spatial memory Working memory Hippocampus L-LTP FosB 


Author Contributions

Ying-Li, Tian-Ming Gao, and Jian-Ming Li contributed to study concept and design; Ying-Li, Qiang-Long You, Sheng-Rong Zhang, Wei-Yuan Huang, Wen-Jun Zou, Wei Jie, Shu-Ji Li, Ji-Hong Liu, Chuang-Ye Lv, Jin Cong, and Yu-Ying Hu contributed to data acquisition; Ying-Li, Tian-Ming Gao, and Jian-Ming Li contributed to data analysis and interpretation; Ying-Li, Tian-Ming Gao, and Jian-Ming Li contributed to manuscript drafting; Tian-Ming Gao and Jian-Ming Li contributed to funding obtaining and study supervision.

Compliance with Ethical Standards

Grant Support

This work was supported by the National Nature Science Foundation of China (Grants 81,525,020, 81,502,033, 81,272,300, 31570753, 31430032 and U1201225).

Conflict of Interest

The authors declare that they have no conflicts of interest.

Supplementary material

12035_2017_531_MOESM1_ESM.docx (220 kb)
Fig. S1 Heterozygous Satb2 mutant mice show normal locomotor activity and fear memory. (A and B) Open field test. Distance traveled (A) and time in center (B) for Satb2+/+ mice (n = 16) and Satb2+/− mice (n = 14) in 30 min. (C) Novel object recognition test. Satb2+/+ mice (n = 15) and Satb2+/− mice (n = 20) had similar preference to the novel object at 1 h after memorizing the circumstance and old objects. (D and E) Contextual fear conditioning. Similar freezing time of Satb2+/+ mice (n = 9) and Satb2+/− mice (n = 10) was showed during fear-acquisition period (D). After 24 h, intact contextual fear memory of Satb2+/− mice was showed in memory retrieval phase (E). (F) Y-maze. Correct trials of Satb2+/− mice (n = 15) were similar with Satb2+/+ mice (n = 16) during spontaneous exploration in Y-shaped apparatus. Data shown are represented as mean ± SEM. *P < 0.05. **P < 0.01. ***P < 0.001. (DOCX 219 kb)
12035_2017_531_MOESM2_ESM.docx (269 kb)
Fig. S2 Heterozygous deletion of Satb2 in mice leads to impaired social memory. (A) Self-grooming time for Satb2+/+ mice (n = 17) and Satb2+/− mice (n = 15) was similar in 10 min. (B–F) Three-chambered social test. Three divided chambers were named left, middle, and right ones. During the first 10-min habituation phase, time spent in left and right chambers was close both in Satb2+/+ mice (n = 14) and Satb2+/− mice (n = 12) (B). During the second 10-min phase, time spent in left chamber with stranger 1 was higher than right chamber with an empty box both in Satb2+/+ mice and Satb2+/− mice (C) and the sniffing time spent on stranger 1 was also higher than that on the empty box (D). During the third 10-min phase, time spent in left chamber with stranger 1 and right chamber with stranger 2 were similar in Satb2+/− mice (E), and Satb2+/− mice also did not show an increase in the sniffing time spent on stranger 2 (F). Data shown are represented as mean ± SEM. *P < 0.05. **P < 0.01. ***P < 0.001. (DOCX 268 kb)
12035_2017_531_MOESM3_ESM.docx (757 kb)
Fig. S3 Hyperactivity and aberrant prefrontal cortex are showed when the expression of Satb2 in pyramidal neurons is deleted in mice. (A and B) Open field test. Distance traveled (A) and time in center (B) for Satb2fl/fl mice and Cre+Satb2fl/fl mice in 30 min. Cre+Satb2fl/fl mice showed increased locomotor activities (A) and increased time in center (B). (C) Anti-Neun antibody was used to incubate prefrontal cortex slices of Satb2fl/fl mice and Cre+Satb2fl/fl mice. The green fluorescence represented Neun positive cells. The white boxes with dotted lines showed the aberrant neuronal distributions in Cre+Satb2fl/fl mice. Data shown are represented as mean ± SEM. *P < 0.05. **P < 0.01. ***P < 0.001. (DOCX 756 kb)
12035_2017_531_MOESM4_ESM.docx (216 kb)
Fig. S4 Satb2 regulates FosB directly in the hippocampus of mice. (A–C) ChIP-PCR assay was used to find out the genomic binding sites for Fos (A), FosB (B), and Egr2 (C). ChIP was carried out with either anti-Satb2 antibody or anti-RNA pol II antibody or anti-IgG antibody. Predicted Satb2-binding loci are marked by red squares under the genomic sequence. Exons for each genomic sequence are marked by green boxes and translation initiation sites are marked by black arrows. Satb2 could bind with FosB on the site numbered 1. (DOCX 215 kb)
12035_2017_531_MOESM5_ESM.docx (33 kb)
ESM 1 (DOCX 33 kb)


  1. 1.
    Gyorgy AB, Szemes M, de Juan RC, Tarabykin V, Agoston DV (2008) SATB2 interacts with chromatin-remodeling molecules in differentiating cortical neurons. Eur J Neurosci 27(4):865–873. doi: 10.1111/j.1460-9568.2008.06061.x CrossRefPubMedGoogle Scholar
  2. 2.
    Britanova O, Akopov S, Lukyanov S, Gruss P, Tarabykin V (2005) Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur J Neurosci 21(3):658–668. doi: 10.1111/j.1460-9568.2005.03897.x CrossRefPubMedGoogle Scholar
  3. 3.
    Fitz Patrick DR, Carr IM, McLaren L, Leek JP, Wightman P, Williamson K, Gautier P, McGill N et al (2003) Identification of SATB2 as the cleft palate gene on 2q32-q33. Hum Mol Genet 12(19):2491–2501. doi: 10.1093/hmg/ddg248 CrossRefGoogle Scholar
  4. 4.
    Brewer CM, Leek JP, Green AJ, Holloway S, Bonthron DT, Markham AF, FitzPatrick DR (1999) A locus for isolated cleft palate, located on human chromosome 2q32. Am J Hum Genet 65(2):387–396. doi: 10.1086/302498 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Tegay DH, Chan KK, Leung L, Wang C, Burkett S, Stone G, Stanyon R, Toriello HV et al (2009) Toriello-Carey syndrome in a patient with a de novo balanced translocation [46,XY,t(2;14)(q33;q22)] interrupting SATB2. Clin Genet 75(3):259–264. doi: 10.1111/j.1399-0004.2008.01145.x CrossRefPubMedGoogle Scholar
  6. 6.
    Talkowski ME, Rosenfeld JA, Blumenthal I, Pillalamarri V, Chiang C, Heilbut A, Ernst C, Hanscom C et al (2012) Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell 149(3):525–537. doi: 10.1016/j.cell.2012.03.028 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Balasubramanian M, Smith K, Basel-Vanagaite L, Feingold MF, Brock P, Gowans GC, Vasudevan PC, Cresswell L et al (2011) Case series: 2q33.1 microdeletion syndrome—further delineation of the phenotype. J Med Genet 48(5):290–298. doi: 10.1136/jmg.2010.084491 CrossRefPubMedGoogle Scholar
  8. 8.
    Van Buggenhout G, Van Ravenswaaij-Arts C, Mc Maas N, Thoelen R, Vogels A, Smeets D, Salden I, Matthijs G et al (2005) The del(2)(q32.2q33) deletion syndrome defined by clinical and molecular characterization of four patients. European journal of medical genetics 48(3):276–289. doi: 10.1016/j.ejmg.2005.05.005 CrossRefPubMedGoogle Scholar
  9. 9.
    de Ravel TJ, Balikova I, Thiry P, Vermeesch JR, Frijns JP (2009) Another patient with a de novo deletion further delineates the 2q33.1 microdeletion syndrome. European journal of medical genetics 52(2–3):120–122. doi: 10.1016/j.ejmg.2009.01.002 CrossRefPubMedGoogle Scholar
  10. 10.
    Zarate YA, Perry H, Ben-Omran T, Sellars EA, Stein Q, Almureikhi M, Simmons K, Klein O et al (2015) Further supporting evidence for the SATB2-associated syndrome found through whole exome sequencing. Am J Med Genet A 167A(5):1026–1032. doi: 10.1002/ajmg.a.36849 CrossRefPubMedGoogle Scholar
  11. 11.
    Docker D, Schubach M, Menzel M, Munz M, Spaich C, Biskup S, Bartholdi D (2014) Further delineation of the SATB2 phenotype. European journal of human genetics: EJHG 22(8):1034–1039. doi: 10.1038/ejhg.2013.280 CrossRefPubMedGoogle Scholar
  12. 12.
    Lee JS, Yoo Y, Lim BC, Kim KJ, Choi M, Chae JH (2016) SATB2-associated syndrome presenting with Rett-like phenotypes. Clin Genet 89(6):728–732. doi: 10.1111/cge.12698 CrossRefPubMedGoogle Scholar
  13. 13.
    Leoyklang P, Suphapeetiporn K, Siriwan P, Desudchit T, Chaowanapanja P, Gahl WA, Shotelersuk V (2007) Heterozygous nonsense mutation SATB2 associated with cleft palate, osteoporosis, and cognitive defects. Hum Mutat 28(7):732–738. doi: 10.1002/humu.20515 CrossRefPubMedGoogle Scholar
  14. 14.
    Britanova O, de Juan RC, Cheung A, Kwan KY, Schwark M, Gyorgy A, Vogel T, Akopov S et al (2008) Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57(3):378–392. doi: 10.1016/j.neuron.2007.12.028 CrossRefPubMedGoogle Scholar
  15. 15.
    Alcamo EA, Chirivella L, Dautzenberg M, Dobreva G, Farinas I, Grosschedl R, McConnell SK (2008) Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57(3):364–377. doi: 10.1016/j.neuron.2007.12.012 CrossRefPubMedGoogle Scholar
  16. 16.
    Srivatsa S, Parthasarathy S, Britanova O, Bormuth I, Donahoo AL, Ackerman SL, Richards LJ, Tarabykin V (2014) Unc5C and DCC act downstream of Ctip2 and Satb2 and contribute to corpus callosum formation. Nat Commun 5:3708. doi: 10.1038/ncomms4708 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Bonneau D, Toutain A, Laquerriere A, Marret S, Saugier-Veber P, Barthez MA, Radi S, Biran-Mucignat V et al (2002) X-linked lissencephaly with absent corpus callosum and ambiguous genitalia (XLAG): clinical, magnetic resonance imaging, and neuropathological findings. Ann Neurol 51(3):340–349CrossRefPubMedGoogle Scholar
  18. 18.
    Huang Y, Song NN, Lan W, Hu L, Su CJ, Ding YQ, Zhang L (2013) Expression of transcription factor Satb2 in adult mouse brain. Anat Rec 296(3):452–461. doi: 10.1002/ar.22656 CrossRefGoogle Scholar
  19. 19.
    Jaitner C, Reddy C, Abentung A, Whittle N, Rieder D, Delekate A, Korte M, Jain G et al (2016) Satb2 determines miRNA expression and long-term memory in the adult central nervous system. elife 5:e17361CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Burgess N, Maguire EA, O'Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641CrossRefPubMedGoogle Scholar
  21. 21.
    Nyberg L, McIntosh AR, Cabeza R, Habib R, Houle S, Tulving E (1996) General and specific brain regions involved in encoding and retrieval of events: what, where, and when. Proc Natl Acad Sci 93(20):11280–11285CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M et al (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474(7351):337–342. doi: 10.1038/nature10163 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Nestler EJ, Kelz MB, Chen J (1999) ΔFosB: a molecular mediator of long-term neural and behavioral plasticity. Brain Res 835(1):10–17CrossRefPubMedGoogle Scholar
  24. 24.
    Eagle AL, Gajewski PA, Yang M, Kechner ME, Al Masraf BS, Kennedy PJ, Wang H et al (2015) Experience-dependent induction of hippocampal ΔFosB controls learning. J Neurosci 35(40):13773–13783CrossRefPubMedGoogle Scholar
  25. 25.
    Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD et al (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13(1):133–140CrossRefPubMedGoogle Scholar
  26. 26.
    Li B, Jie W, Huang L, Wei P, Li S, Luo Z, Friedman AK, Meredith AL et al (2014) Nuclear BK channels regulate gene expression via the control of nuclear calcium signaling. Nat Neurosci 17(8):1055–1063. doi: 10.1038/nn.3744 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Li Y, Liu Y-H, Hu Y-Y, Chen L, Li J-M (2016) Special AT-rich sequence-binding protein 2 acts as a negative regulator of stemness in colorectal cancer cells. World J Gastroenterol 22(38):8528CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1(2):848–858. doi: 10.1038/nprot.2006.116 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Deacon RM, Rawlins JN (2006) T-maze alternation in the rodent. Nat Protoc 1(1):7–12. doi: 10.1038/nprot.2006.2 CrossRefPubMedGoogle Scholar
  30. 30.
    Cao X, Li LP, Wang Q, Wu Q, Hu HH, Zhang M, Fang YY, Zhang J et al (2013) Astrocyte-derived ATP modulates depressive-like behaviors. Nat Med 19(6):773–777. doi: 10.1038/nm.3162 CrossRefPubMedGoogle Scholar
  31. 31.
    Konsman J-P (2003) The mouse brain in stereotaxic coordinates: (Deluxe) by Paxinos G. and Franklin, KBJ, Academic Press, New York, 2001, ISBN 0–12-547637-X. PergamonGoogle Scholar
  32. 32.
    Liu JH, You QL, Wei MD, Wang Q, Luo ZY, Lin S, Huang L, Li SJ et al (2015) Social isolation during adolescence strengthens retention of fear memories and facilitates induction of late-phase long-term potentiation. Mol Neurobiol 52(3):1421–1429. doi: 10.1007/s12035-014-8917-0 CrossRefPubMedGoogle Scholar
  33. 33.
    Šišková Z, Justus D, Kaneko H, Friedrichs D, Henneberg N, Beutel T, Pitsch J, Schoch S et al (2014) Dendritic structural degeneration is functionally linked to cellular hyperexcitability in a mouse model of Alzheimer’s disease. Neuron 84(5):1023–1033. doi: 10.1016/j.neuron.2014.10.024 CrossRefPubMedGoogle Scholar
  34. 34.
    Balamotis MA, Tamberg N, Woo YJ, Li J, Davy B, Kohwi-Shigematsu T, Kohwi Y (2012) Satb1 ablation alters temporal expression of immediate early genes and reduces dendritic spine density during postnatal brain development. Mol Cell Biol 32(2):333–347. doi: 10.1128/MCB.05917-11 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Jain R, Iglesias N, Moazed D (2016) Distinct functions of argonaute slicer in siRNA maturation and heterochromatin formation. Mol Cell 63(2):191–205. doi: 10.1016/j.molcel.2016.05.039 CrossRefPubMedGoogle Scholar
  36. 36.
    Casanova E, Fehsenfeld S, Mantamadiotis T, Lemberger T, Greiner E, Stewart AF, Schutz G (2001) A CamKIIalpha iCre BAC allows brain-specific gene inactivation. Genesis 31(1):37–42CrossRefPubMedGoogle Scholar
  37. 37.
    Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39CrossRefPubMedGoogle Scholar
  38. 38.
    Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R (2014) Engineering a memory with LTD and LTP. Nature 511:348–352. doi: 10.1038/nature13294
  39. 39.
    Lu W-Y, Man H-Y, Ju W, Trimble WS, MacDonald JF, Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29(1):243–254CrossRefPubMedGoogle Scholar
  40. 40.
    Kandel ER, Dudai Y, Mayford MR (2014) The molecular and systems biology of memory. Cell 157(1):163–186. doi: 10.1016/j.cell.2014.03.001 CrossRefPubMedGoogle Scholar
  41. 41.
    Izquierdo I, Bevilaqua LM, Rossato JI, Da Silva WC, Bonini J, Medina JH, Cammarota M (2008) The molecular cascades of long-term potentiation underlie memory consolidation of one-trial avoidance in the CA1 region of the dorsal hippocampus, but not in the basolateral amygdala or the neocortex. Neurotox Res 14(2–3):273–294CrossRefPubMedGoogle Scholar
  42. 42.
    Okuno H (2011) Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neurosci Res 69(3):175–186. doi: 10.1016/j.neures.2010.12.007 CrossRefPubMedGoogle Scholar
  43. 43.
    Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, Layer LE, Kvello A, Reschke M et al (2003) Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23(27):9116–9122PubMedGoogle Scholar
  44. 44.
    Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A et al (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52(3):437–444. doi: 10.1016/j.neuron.2006.08.024 CrossRefPubMedGoogle Scholar
  45. 45.
    Jones M, Errington M, French P, Fine A, Bliss T, Garel S, Charnay P, Bozon B et al (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4(3):289–296CrossRefPubMedGoogle Scholar
  46. 46.
    McClung CA, Ulery PG, Perrotti LI, Zachariou V, Berton O, Nestler EJ (2004) DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res Mol Brain Res 132(2):146–154. doi: 10.1016/j.molbrainres.2004.05.014 CrossRefPubMedGoogle Scholar
  47. 47.
    Zhang L, Song NN, Chen JY, Huang Y, Li H, Ding YQ (2012) Satb2 is required for dendritic arborization and soma spacing in mouse cerebral cortex. Cereb Cortex 22(7):1510–1519. doi: 10.1093/cercor/bhr215 CrossRefPubMedGoogle Scholar
  48. 48.
    Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB (2008) Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57(2):290–302. doi: 10.1016/j.neuron.2007.11.034 CrossRefPubMedGoogle Scholar
  49. 49.
    Suh J, Rivest AJ, Nakashiba T, Tominaga T, Tonegawa S (2011) Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 334(6061):1415–1420. doi: 10.1126/science.1210125 CrossRefPubMedGoogle Scholar
  50. 50.
    Kitamura T, Pignatelli M, Suh J, Kohara K, Yoshiki A, Abe K, Tonegawa S (2014) Island cells control temporal association memory. Science 343(6173):896–901. doi: 10.1126/science.1244634 CrossRefPubMedGoogle Scholar
  51. 51.
    Witter MP, Amaral DG (1991) Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J Comp Neurol 307(3):437–459CrossRefPubMedGoogle Scholar
  52. 52.
    Meyer D, Bonhoeffer T, Scheuss V (2014) Balance and stability of synaptic structures during synaptic plasticity. Neuron 82(2):430–443. doi: 10.1016/j.neuron.2014.02.031 CrossRefPubMedGoogle Scholar
  53. 53.
    Lu Y, Christian K, Lu B (2008) BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89(3):312–323. doi: 10.1016/j.nlm.2007.08.018 CrossRefPubMedGoogle Scholar
  54. 54.
    Barco A, Patterson SL, Alarcon JM, Gromova P, Mata-Roig M, Morozov A, Kandel ER (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48(1):123–137. doi: 10.1016/j.neuron.2005.09.005 CrossRefPubMedGoogle Scholar
  55. 55.
    Miyashita T, Kubik S, Lewandowski G, Guzowski JF (2008) Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol Learn Mem 89(3):269–284CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Ying Li
    • 1
    • 2
    • 3
  • Qiang-Long You
    • 4
  • Sheng-Rong Zhang
    • 4
  • Wei-Yuan Huang
    • 4
  • Wen-Jun Zou
    • 4
  • Wei Jie
    • 4
  • Shu-Ji Li
    • 4
  • Ji-Hong Liu
    • 4
  • Chuang-Ye Lv
    • 5
  • Jin Cong
    • 4
  • Yu-Ying Hu
    • 2
  • Tian-Ming Gao
    • 4
    Email author
  • Jian-Ming Li
    • 1
    • 2
    • 6
    Email author
  1. 1.Department of PathologySun Yat-Sen Memorial HospitalGuangzhouPeople’s Republic of China
  2. 2.Department of Pathology, Nanfang HospitalSouthern Medical UniversityGuangzhouPeople’s Republic of China
  3. 3.Department of PathologyChancheng Central HospitalFoshanPeople’s Republic of China
  4. 4.State Key Laboratory of Organ Failure Research, Key Laboratory of Psychiatric Disorders of Guangdong Province, Department of Neurobiology, School of Basic Medical SciencesSouthern Medical UniversityGuangzhouPeople’s Republic of China
  5. 5.College of Clinical MedicalSouthern Medical UniversityGuangzhouPeople’s Republic of China
  6. 6.Department of PathologySoochow University Medical SchoolSuzhouPeople’s Republic of China

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