Skip to main content

Advertisement

SpringerLink
Log in

Expression of Macrophage Migration Inhibitory Factor in the Mouse Neocortex and Posterior Piriform Cortices During Postnatal Development

  • Original Research
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Macrophage migration inhibitory factor (MIF) functions as a pleiotropic protein, participating in a vast array of cellular and biological processes. Abnormal expression of MIF has been implicated in many neurological diseases, including Parkinson’s disease, epilepsy, Alzheimer’s Disease, stroke, and neuropathic pain. However, the expression patterns of mif transcript and MIF protein from the early postnatal period through adulthood in the mouse brain are still poorly understood. We therefore investigated the temporal and spatial expression of MIF in the mouse neocortex during postnatal development in detail and partially in posterior piriform cortices (pPC). As determined by quantitative real-time PCR (qPCR), mif transcript gradually increased during development, with the highest level noted at postnatal day 30 (P30) followed by a sharp decline at P75. In contrast, Western blotting results showed that MIF increased constantly from P7 to P75. The highest level of MIF was at P75, while the lowest level of MIF was at P7. Immunofluorescence histochemistry revealed that MIF-immunoreactive (ir) cells were within the entire depth of the developed neocortex, and MIF was heterogeneously distributed among cortical cells, especially at P7, P14, P30, and P75; MIF was abundant in the pyramidal layer within pPC. Double immunostaining showed that all the mature neurons were MIF-ir and all the intensely stained MIF-ir cells were parvalbumin positive (Pv +) at adult. Moreover, it was demonstrated that MIF protein localized in the perikaryon, processes, presynaptic structures, and the nucleus in neurons. Taken together, the developmentally regulated expression and the subcellular localization of MIF should form a platform for an analysis of MIF neurodevelopmental biology and MIF-related nerve diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Alexander JK, Cox GM, Tian JB, Zha AM, Wei P, Kigerl KA, Reddy MK, Dagia NM, Sielecki T, Zhu MX, Satoskar AR, McTigue DM, Whitacre CC, Popovich PG (2012) Macrophage migration inhibitory factor (MIF) is essential for inflammatory and neuropathic pain and enhances pain in response to stress. Exp Neurol 236(2):351–362. doi:10.1016/j.expneurol.2012.04.018

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D (2003) Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100(7):3889–3894. doi:10.1073/pnas.0635171100

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bacher M, Meinhardt A, Lan HY, Dhabhar FS, Mu W, Metz CN, Chesney JA, Gemsa D, Donnelly T, Atkins RC, Bucala R (1998) MIF expression in the rat brain: implications for neuronal function. Mol Med 4(4):217–230

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bacher M, Deuster O, Aljabari B, Egensperger R, Neff F, Jessen F, Popp J, Noelker C, Reese JP, Al-Abed Y, Dodel R (2010) The role of macrophage migration inhibitory factor in Alzheimer’s disease. Mol Med 16(3–4):116–121. doi:10.2119/molmed.2009.00123

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bank LM, Bianchi LM, Ebisu F, Lerman-Sinkoff D, Smiley EC, Shen YC, Ramamurthy P, Thompson DL, Roth TM, Beck CR, Flynn M, Teller RS, Feng L, Llewellyn GN, Holmes B, Sharples C, Coutinho-Budd J, Linn SA, Chervenak AP, Dolan DF, Benson J, Kanicki A, Martin CA, Altschuler R, Koch AE, Jewett EM, Germiller JA, Barald KF (2012) Macrophage migration inhibitory factor acts as a neurotrophin in the developing inner ear. Development 139(24):4666–4674. doi:10.1242/dev.066647

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bloom BR, Bennett B (1966) Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153(3731):80–82

    Article  PubMed  CAS  Google Scholar 

  • Calandra T, Roger T (2003) Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3(10):791–800. doi:10.1038/nri1200

    Article  PubMed  CAS  Google Scholar 

  • Calu DJ, Roesch MR, Stalnaker TA, Schoenbaum G (2007) Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb Cortex 17(6):1342–1349. doi:10.1093/cercor/bhl045

    Article  PubMed  PubMed Central  Google Scholar 

  • Chklovskii DB, Mel BW, Svoboda K (2004) Cortical rewiring and information storage. Nature 431(7010):782–788. doi:10.1038/nature03012

    Article  PubMed  CAS  Google Scholar 

  • Cho RY, Konecky RO, Carter CS (2006) Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci USA 103(52):19878–19883. doi:10.1073/pnas.0609440103

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Conboy L, Varea E, Castro JE, Sakouhi-Ouertatani H, Calandra T, Lashuel HA, Sandi C (2011) Macrophage migration inhibitory factor is critically involved in basal and fluoxetine-stimulated adult hippocampal cell proliferation and in anxiety, depression, and memory-related behaviors. Molecular psychiatry 16(5):533–547. doi:10.1038/mp.2010.15

    Article  PubMed  CAS  Google Scholar 

  • Conroy H, Mawhinney L, Donnelly SC (2010) Inflammation and cancer: macrophage migration inhibitory factor (MIF)–the potential missing link. QJM 103(11):831–836. doi:10.1093/qjmed/hcq148

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Danis O, Demir S, Gunel A, Aker RG, Gulcebi M, Onat F, Ogan A (2011) Changes in intracellular protein expression in cortex, thalamus and hippocampus in a genetic rat model of absence epilepsy. Brain Res Bull 84(6):381–388. doi:10.1016/j.brainresbull.2011.02.002

    Article  PubMed  CAS  Google Scholar 

  • Donato F, Rompani SB, Caroni P (2013) Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504(7479):272–276. doi:10.1038/nature12866

    Article  PubMed  CAS  Google Scholar 

  • Eickhoff R, Wilhelm B, Renneberg H, Wennemuth G, Bacher M, Linder D, Bucala R, Seitz J, Meinhardt A (2001) Purification and characterization of macrophage migration inhibitory factor as a secretory protein from rat epididymis: evidences for alternative release and transfer to spermatozoa. Mol Med 7(1):27–35

    PubMed  CAS  PubMed Central  Google Scholar 

  • Friberg M, von Rohr P, Gonnet G (2004) Limitations of codon adaptation index and other coding DNA-based features for prediction of protein expression in Saccharomyces cerevisiae. Yeast 21(13):1083–1093. doi:10.1002/yea.1150

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto S (1997) Identification of macrophage migration inhibitory factor (MIF) in rat spinal cord and its kinetics on experimental spinal cord injury. [Hokkaido igaku zasshi] 72(4):409–430

    CAS  Google Scholar 

  • Gibbings DJ, Ghetu AF, Dery R, Befus AD (2008) Macrophage migration inhibitory factor has a MHC class I-like motif and function. Scand J Immunol 67(2):121–132. doi:10.1111/j.1365-3083.2007.02046.x

    Article  PubMed  CAS  Google Scholar 

  • Gottfried JA, Winston JS, Dolan RJ (2006) Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49(3):467–479. doi:10.1016/j.neuron.2006.01.007

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara A, Pal SK, Sato TF, Wienisch M, Murthy VN (2012) Optophysiological analysis of associational circuits in the olfactory cortex. Front Neural Circuits 6:18. doi:10.3389/fncir.2012.00018

    Article  PubMed  PubMed Central  Google Scholar 

  • Harrison RA, Sumners C (2009) Redox regulation of macrophage migration inhibitory factor expression in rat neurons. Biochem Biophys Res Commun 390(1):171–175. doi:10.1016/j.bbrc.2009.09.112

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Inacio AR, Ruscher K, Wieloch T (2011) Enriched environment downregulates macrophage migration inhibitory factor and increases parvalbumin in the brain following experimental stroke. Neurobiol Dis 41(2):270–278. doi:10.1016/j.nbd.2010.09.015

    Article  PubMed  CAS  Google Scholar 

  • Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324(5924):218–223. doi:10.1126/science.1168978

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson DM, Illig KR, Behan M, Haberly LB (2000) New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that “primary” olfactory cortex functions like “association” cortex in other sensory systems. J Neurosci 20(18):6974–6982

    PubMed  CAS  Google Scholar 

  • Kadohisa M, Wilson DA (2006) Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci USA 103(41):15206–15211. doi:10.1073/pnas.0604313103

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kamimura A, Kamachi M, Nishihira J, Ogura S, Isobe H, Dosaka-Akita H, Ogata A, Shindoh M, Ohbuchi T, Kawakami Y (2000) Intracellular distribution of macrophage migration inhibitory factor predicts the prognosis of patients with adenocarcinoma of the lung. Cancer 89(2):334–341

    Article  PubMed  CAS  Google Scholar 

  • Kato HK, Gillet SN, Peters AJ, Isaacson JS, Komiyama T (2013) Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80(5):1218–1231. doi:10.1016/j.neuron.2013.08.036

    Article  PubMed  CAS  Google Scholar 

  • Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Juttner S, Brunner H, Bernhagen J (1998) Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol 280(1):85–102. doi:10.1006/jmbi.1998.1864

    Article  PubMed  CAS  Google Scholar 

  • Krockenberger M, Dombrowski Y, Weidler C, Ossadnik M, Honig A, Hausler S, Voigt H, Becker JC, Leng L, Steinle A, Weller M, Bucala R, Dietl J, Wischhusen J (2008) Macrophage migration inhibitory factor contributes to the immune escape of ovarian cancer by down-regulating NKG2D. J Immunol 180(11):7338–7348

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Le Roux N, Cabezas C, Bohm UL, Poncer JC (2013) Input-specific learning rules at excitatory synapses onto hippocampal parvalbumin-expressing interneurons. J Physiol 591(Pt 7):1809–1822. doi:10.1113/jphysiol.2012.245852

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee CY, Su MJ, Huang CY, Chen MY, Hsu HC, Lin CY, Tang CH (2012) Macrophage migration inhibitory factor increases cell motility and up-regulates alphavbeta3 integrin in human chondrosarcoma cells. J Cell Biochem 113(5):1590–1598. doi:10.1002/jcb.24027

    PubMed  CAS  Google Scholar 

  • Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6(4):312–324. doi:10.1038/nrn1648

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Chen G, Zhang W, Zhu JY, Lin ZQ, Gong ZC, Wang FQ, Jia J, Sun ZJ, Zhao YF (2013) Overexpression of macrophage migration inhibitory factor in adenoid cystic carcinoma: correlation with enhanced metastatic potential. J Cancer Res Clin Oncol 139(2):287–295. doi:10.1007/s00432-012-1330-z

    Article  PubMed  CAS  Google Scholar 

  • Llamas-Covarrubias MA, Valle Y, Bucala R, Navarro-Hernandez RE, Palafox-Sanchez CA, Padilla-Gutierrez JR, Parra-Rojas I, Bernard-Medina AG, Reyes-Castillo Z, Munoz-Valle JF (2013) Macrophage migration inhibitory factor (MIF): genetic evidence for participation in early onset and early stage rheumatoid arthritis. Cytokine 61(3):759–765. doi:10.1016/j.cyto.2012.12.032

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Miracco C, De Nisi MC, Arcuri F, Cosci E, Pacenti L, Toscano M, Lalinga AV, Biagioli M, Rubegni P, Vatti R, Maellaro E, Del Bello B, Massi D, Luzi P, Tosi P (2006) Macrophage migration inhibitory factor protein and mRNA expression in cutaneous melanocytic tumours. Int J Oncol 28(2):345–352

    PubMed  CAS  Google Scholar 

  • Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L, Mizrahi A (2013) Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80(5):1232–1245. doi:10.1016/j.neuron.2013.08.027

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Morimoto T, Nishihira J, Kohgo T (2003) Immunohistochemical localization of macrophage migration inhibitory factor (MIF) in human gingival tissue and its pathophysiological functions. Histochem Cell Biol 120(4):293–298. doi:10.1007/s00418-003-0571-y

    Article  PubMed  CAS  Google Scholar 

  • Mouly AM, Gervais R (2002) Polysynaptic potentiation at different levels of rat olfactory pathways following learning. Learn Mem 9(2):66–75. doi:10.1101/lm.45602

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicoletti A, Fagone P, Donzuso G, Mangano K, Dibilio V, Caponnetto S, Bendtzen K, Zappia M, Nicoletti F (2011) Parkinson’s disease is associated with increased serum levels of macrophage migration inhibitory factor. Cytokine 55(2):165–167. doi:10.1016/j.cyto.2011.03.027

    Article  PubMed  CAS  Google Scholar 

  • Nishibori M, Nakaya N, Tahara A, Kawabata M, Mori S, Saeki K (1996) Presence of macrophage migration inhibitory factor (MIF) in ependyma, astrocytes and neurons in the bovine brain. Neurosci Lett 213(3):193–196

    Article  PubMed  CAS  Google Scholar 

  • Nishibori M, Nakaya N, Mori S, Saeki K (1997) Immunohistochemical localization of macrophage migration inhibitory factor (MIF) in tanycytes, subcommissural organ and choroid plexus in the rat brain. Brain Res 758(1–2):259–262

    Article  PubMed  CAS  Google Scholar 

  • Nishihira J, Koyama Y, Mizue Y (1998) Identification of macrophage migration inhibitory factor (MIF) in human vascular endothelial cells and its induction by lipopolysaccharide. Cytokine 10(3):199–205

    Article  PubMed  CAS  Google Scholar 

  • Nishio Y, Koda M, Hashimoto M, Kamada T, Koshizuka S, Yoshinaga K, Onodera S, Nishihira J, Okawa A, Yamazaki M (2009) Deletion of macrophage migration inhibitory factor attenuates neuronal death and promotes functional recovery after compression-induced spinal cord injury in mice. Acta Neuropathol 117(3):321–328. doi:10.1007/s00401-008-0476-x

    Article  PubMed  CAS  Google Scholar 

  • Ogata A, Nishihira J, Suzuki T, Nagashima K, Tashiro K (1998) Identification of macrophage migration inhibitory factor mRNA expression in neural cells of the rat brain by in situ hybridization. Neurosci Lett 246(3):173–177

    Article  PubMed  CAS  Google Scholar 

  • Oyama R, Yamamoto H, Titani K (2000) Glutamine synthetase, hemoglobin alpha-chain, and macrophage migration inhibitory factor binding to amyloid beta-protein: their identification in rat brain by a novel affinity chromatography and in Alzheimer’s disease brain by immunoprecipitation. Biochim Biophys Acta 1479(1–2):91–102

    Article  PubMed  CAS  Google Scholar 

  • Popp J, Bacher M, Kolsch H, Noelker C, Deuster O, Dodel R, Jessen F (2009) Macrophage migration inhibitory factor in mild cognitive impairment and Alzheimer’s disease. J Psychiatr Res 43(8):749–753. doi:10.1016/j.jpsychires.2008.10.006

    Article  PubMed  Google Scholar 

  • Pyle ME, Korbonits M, Gueorguiev M, Jordan S, Kola B, Morris DG, Meinhardt A, Powell MP, Claret FX, Zhang Q, Metz C, Bucala R, Grossman AB (2003) Macrophage migration inhibitory factor expression is increased in pituitary adenoma cell nuclei. J Endocrinol 176(1):103–110

    Article  PubMed  CAS  Google Scholar 

  • Raineki C, Shionoya K, Sander K, Sullivan RM (2009) Ontogeny of odor-LiCl vs. odor-shock learning: similar behaviors but divergent ages of functional amygdala emergence. Learn Mem 16(2):114–121. doi:10.1101/lm.977909

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sevelinges Y, Gervais R, Messaoudi B, Granjon L, Mouly AM (2004) Olfactory fear conditioning induces field potential potentiation in rat olfactory cortex and amygdala. Learn Mem 11(6):761–769. doi:10.1101/lm.83604

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen YC, Thompson DL, Kuah MK, Wong KL, Wu KL, Linn SA, Jewett EM, Shu-Chien AC, Barald KF (2012) The cytokine macrophage migration inhibitory factor (MIF) acts as a neurotrophin in the developing inner ear of the zebrafish, Danio rerio. Dev Biol 363(1):84–94. doi:10.1016/j.ydbio.2011.12.023

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Singh A, Leng L, Fan J, Gajda M, Brauer R, Fingerle-Rowson G, Bucala R, Illges H (2013) Macrophage-derived, macrophage migration inhibitory factor (MIF) is necessary to induce disease in the K/BxN serum-induced model of arthritis. Rheumatol Int 33(9):2301–2308. doi:10.1007/s00296-013-2713-4

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Song J, Sun J, Moss J, Wen Z, Sun GJ, Hsu D, Zhong C, Davoudi H, Christian KM, Toni N, Ming GL, Song H (2013) Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus. Nat Neurosci 16(12):1728–1730. doi:10.1038/nn.3572

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW (2004) Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA 101(49):17288–17293. doi:10.1073/pnas.0406074101

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sun HW, Bernhagen J, Bucala R, Lolis E (1996a) Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc Natl Acad Sci USA 93(11):5191–5196

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sun HW, Swope M, Cinquina C, Bedarkar S, Bernhagen J, Bucala R, Lolis E (1996b) The subunit structure of human macrophage migration inhibitory factor: evidence for a trimer. Protein Eng 9(8):631–635

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Sugimoto H, Nakagawa A, Tanaka I, Nishihira J, Sakai M (1996) Crystal structure of the macrophage migration inhibitory factor from rat liver. Nat Struct Biol 3(3):259–266

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Ogata A, Tashiro K, Nagashima K, Tamura M, Nishihira J (1999) Augmented expression of macrophage migration inhibitory factor (MIF) in the telencephalon of the developing rat brain. Brain Res 816(2):457–462

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Takamura Y, Maeno M, Tochinai S, Iyaguchi D, Tanaka I, Nishihira J, Ishibashi T (2004) Xenopus laevis macrophage migration inhibitory factor is essential for axis formation and neural development. J Biol Chem 279(20):21406–21414. doi:10.1074/jbc.M311416200

    Article  PubMed  CAS  Google Scholar 

  • Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103(4):865–872

    Article  PubMed  CAS  Google Scholar 

  • Tuller T, Waldman YY, Kupiec M, Ruppin E (2010) Translation efficiency is determined by both codon bias and folding energy. Proc Natl Acad Sci USA 107(8):3645–3650. doi:10.1073/pnas.0909910107

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Vedder H, Krieg JC, Gerlach B, Gemsa D, Bacher M (2000) Expression and glucocorticoid regulation of macrophage migration inhibitory factor (MIF) in hippocampal and neocortical rat brain cells in culture. Brain Res 869(1–2):25–30

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Zis O, Ma G, Shan Z, Zhang X, Wang S, Dai C, Zhao J, Lin Q, Lin S, Song W (2009) Upregulation of macrophage migration inhibitory factor gene expression in stroke. Stroke 40(3):973–976. doi:10.1161/STROKEAHA.108.530535

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Nie L, Freeland SJ (2007) The effects of differential gene expression on coding sequence features: analysis by one-way ANOVA. Biochem Biophys Res Commun 358(4):1108–1113. doi:10.1016/j.bbrc.2007.05.043

    Article  PubMed  CAS  Google Scholar 

  • Xiong CJ, Huang B, Zhou Y, Cun YP, Liu LT, Wang J, Li CQ, Pan Y, Wang H (2012) Macrophage migration inhibitory factor inhibits the migration of cartilage end plate-derived stem cells by reacting with CD74. PLoS ONE 7(8):e43984. doi:10.1371/journal.pone.0043984

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by National High Technology Research and Development Program of China (863 Program) (No.2011AA10A208) and Foundation for Special Talent of NWSUAF (No.Z111021101).

Conflict of interest

None.

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Northwest A&F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Wei Zhang, Lingling Li, Jiutao Wang, Lei An, Xinde Hu, Jiongfang Xie, Runchuan Yan, Shulin Chen & Shanting Zhao

Authors
  1. Wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lingling Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiutao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lei An
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinde Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiongfang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Runchuan Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shulin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shanting Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shanting Zhao.

Additional information

Wei Zhang and Lingling Li have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Li, L., Wang, J. et al. Expression of Macrophage Migration Inhibitory Factor in the Mouse Neocortex and Posterior Piriform Cortices During Postnatal Development. Cell Mol Neurobiol 34, 1183–1197 (2014). https://doi.org/10.1007/s10571-014-0094-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-014-0094-1

Keywords

Search

Navigation