Loss of astrocytic leptin signaling worsens experimental autoimmune encephalomyelitis

Brain, Behavior, and Immunity

Volumn 34, Issue , 2013, Pages 98-107

  Mishra, Pramod K ^a,b   Hsuchou, Hung ^a   Ouyang, Suidong ^a   Kastin, Abba J ^a   Wu, Xiaojun ^a,c   Pan, Weihong ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Adenosine; Autoimmunity; EAE; Leptin receptor; Neuroinflammation; Reactive astrogliosis

Indexed keywords

ADENOSINE; CD4 ANTIGEN; INTERLEUKIN 6; LEPTIN; LEPTIN RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOIMMUNITY; BRAIN TISSUE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DEMYELINATION; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; GENE MUTATION; GENE SILENCING; HIPPOCAMPUS; HORMONE RELEASE; IMMUNOPATHOGENESIS; INTRACELLULAR SIGNALING; KNOCKOUT GENE; MOUSE; NERVE CELL CULTURE; NEUROPATHOLOGY; NEUROTRANSMITTER RELEASE; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; WILD TYPE;

ADENOSINE; AUTOIMMUNITY; EAE; LEPTIN RECEPTOR; NEUROINFLAMMATION; REACTIVE ASTROGLIOSIS;

ADENOSINE; ANIMALS; ASTROCYTES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HIPPOCAMPUS; LEUKOCYTES; MICE; MICE, KNOCKOUT; RECEPTORS, LEPTIN; SPINAL CORD;

EID: 84885040008     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.07.176     Document Type: Article

References (53)

1. Angelucci F., Mirabella M., Caggiula M., Frisullo G., Patanella K., Sancricca C., Nociti V., Tonali P.A., Batocchi A.P. Evidence of involvement of leptin and IL-6 peptides in the action of interferon-beta in secondary progressive multiple sclerosis. Peptides 2005, 26:2289-2293.
2. Ayyildiz M., Yildirim M., Agar E., Baltaci A.K. The effect of leptin on penicillin-induced epileptiform activity in rats. Brain Res. Bull. 2006, 68:374-378.
3. Banks W.A., Kastin A.J. Physiological consequences of the passage of peptides across the blood-brain barrier. Rev. Neurosci. 1993, 4:365-372.
4. Banks W.A., Kastin A.J., Huang W., Jaspan J.B., Maness L.M. Leptin enters the brain by a saturable system independent of insulin. Peptides 1996, 17:305-311.
5. Batocchi A.P., Rotondi M., Caggiula M., Frisullo G., Odoardi F., Nociti V., Carella C., Tonali P.A., Mirabella M. Leptin as a marker of multiple sclerosis activity in patients treated with interferon-beta. J. Neuroimmunol. 2003, 139:150-154.
6. Casper K.B., Jones K., McCarthy K.D. Characterization of astrocyte-specific conditional knockouts. Genesis 2007, 45:292-299.
7. Dal Canto M.C., Melvold R.W., Kim B.S., Miller S.D. Two models of multiple sclerosis: experimental allergic encephalomyelitis (EAE) and Theiler's murine encephalomyelitis virus (TMEV) infection. A pathological and immunological comparison. Microsc. Res. Tech. 1995, 32:215-229.
8. De Rosa V., Procaccini C., La C.A., Chieffi P., Nicoletti G.F., Fontana S., Zappacosta S., Matarese G. Leptin neutralization interferes with pathogenic T cell autoreactivity in autoimmune encephalomyelitis. J. Clin. Invest. 2006, 116:447-455.
9. Farr S.A., Banks W.A., Morley J.E. Effects of leptin on memory processing. Peptides 2006, 27:1420-1425.
10. Frisullo G., Mirabella M., Angelucci F., Caggiula M., Morosetti R., Sancricca C., Patanella A.K., Nociti V., Iorio R., Bianco A., Tomassini V., Pozzilli C., Tonali P.A., Matarese G., Batocchi A.P. The effect of disease activity on leptin, leptin receptor and suppressor of cytokine signalling-3 expression in relapsing-remitting multiple sclerosis. J. Neuroimmunol. 2007, 192:174-183.
11. Garza J.C., Guo M., Zhang W., Lu X.Y. Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J. Biol. Chem. 2008, 283:18238-18247.
12. Gimsa U., Oren A., Pandiyan P., Teichmann D., Bechmann I., Nitsch R., Brunner-Weinzierl M.C. Astrocytes protect the CNS: antigen-specific T helper cell responses are inhibited by astrocyte-induced upregulation of CTLA-4 (CD152). J. Mol. Med. (Berl) 2004, 82:364-372.
13. Halassa M.M., Florian C., Fellin T., Munoz J.R., Lee S.Y., Abel T., Haydon P.G., Frank M.G. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 2009, 61:213-219.
14. Haroon F., Drogemuller K., Handel U., Brunn A., Reinhold D., Nishanth G., Mueller W., Trautwein C., Ernst M., Deckert M., Schluter D. Gp130-dependent astrocytic survival is critical for the control of autoimmune central nervous system inflammation. J. Immunol. 2011, 186:6521-6531.
15. Hindinger C., Bergmann C.C., Hinton D.R., Phares T.W., Parra G.I., Hussain S., Savarin C., Atkinson R.D., Stohlman S.A. IFN-gamma signaling to astrocytes protects from autoimmune mediated neurological disability. PLoS One 2012, 7:e42088.
16. Hsuchou H., He Y., Kastin A.J., Tu H., Markadakis E.N., Rogers R.C., Fossier P.B., Pan W. Obesity induces functional astrocytic leptin receptors in hypothalamus. Brain 2009, 132:889-902.
17. Hsuchou H., Kastin A.J., Pan W. Blood-borne metabolic factors in obesity exacerbate injury-induced gliosis. J. Mol. Neurosci. 2012, 47:267-277.
18. Hsuchou H., Kastin A.J., Tu H., Markadakis E.N., Stone K.P., Wang Y., Heymsfield S.B., Chua S.C., Obici S., Magrisso I.J., Pan W. Effects of cell type-specific leptin receptor mutation on leptin transport across the BBB. Peptides 2011, 32:1392-1399.
19. Hsuchou H., Mishra P.K., Kastin A.J., Wu X., Wang Y., Ouyang S., Pan W. Saturable leptin transport across the BBB persists in EAE mice. J. Mol. Neurosci. 2013.
20. Hsuchou H., Pan W., Wu X., Kastin A.J. Cessation of blood-to-brain influx of interleukin-15 during development of EAE. J. Cereb. Blood Flow Metab. 2009, 29:1568-1578.
21. Jayaram B., Khan R.S., Kastin A.J., Hsuchou H., Wu X., Pan W. Protective role of astrocytic leptin signaling against excitotoxicity. J. Mol. Neurosci. 2013, 49:523-530.
22. Jayaram B., Pan W., Wang Y., Hsuchou H., Mace A., Cornelissen-Guillaume G.G., Mishra P.K., Koza R.A., Kastin A.J. Astrocytic leptin-receptor knockout mice show partial rescue of leptin resistance in diet-induced obesity. J. Appl. Physiol. 2013, 114:734-741.
23. Juhler M., Barry D.I., Offner H., Konat G., Klinken L., Paulson O.B. Blood-brain and blood-spinal cord barrier permeability during the course of experimental allergic encephalomyelitis in the rat. Brain Res. 1984, 302:347-355.
24. Kastin A.J., Pan W. Concepts for biologically active peptides. Curr. Pharm. Des. 2010, 16:3390-3400.
25. Kelchtermans H., Billiau A., Matthys P. How interferon-gamma keeps autoimmune diseases in check. Trends Immunol. 2008, 29:479-486.
26. Lanens D., Van der Linden A., Gerrits P.O., 's-Gravenmade E.J. In vitro NMR micro imaging of the spinal cord of chronic relapsing EAE rats. Magn. Reson. Imaging 1994, 12:469-475.
27. Li Q., Powell N., Zhang H., Belevych N., Ching S., Chen Q., Sheridan J., Whitacre C., Quan N. Endothelial IL-1R1 is a critical mediator of EAE pathogenesis. Brain Behav. Immun. 2011, 25:160-167.
28. Matarese G., Carrieri P.B., La C.A., Perna F., Sanna V., De R.V., Aufiero D., Fontana S., Zappacosta S. Leptin increase in multiple sclerosis associates with reduced number of CD4(+)CD25+ regulatory T cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5150-5155.
29. Matarese G., Sanna V., Di Giacomo A., Lord G.M., Howard J.K., Blood S.R., Lechler R.I., Fontana S., Zappacosta S. Leptin potentiates experimental autoimmune encephalomyelitis in SJL female mice and confers susceptibility to males. Eur. J. Immunol. 2001, 31:1324-1332.
30. McColl S.R., Staykova M.A., Wozniak A., Fordham S., Bruce J., Willenborg D.O. Treatment with anti-granulocyte antibodies inhibits the effector phase of experimental autoimmune encephalomyelitis. J. Immunol. 1998, 161:6421-6426.
31. McMinn J.E., Liu S.M., Dragatsis I., Dietrich P., Ludwig T., Eiden S., Chua S.C. An allelic series for the leptin receptor gene generated by CRE and FLP recombinase. Mamm. Genome 2004, 15:677-685.
32. McMinn J.E., Liu S.M., Liu H., Dragatsis I., Dietrich P., Ludwig T., Boozer C.N., Chua S.C. Neuronal deletion of Lepr elicits diabesity in mice without affecting cold tolerance or fertility. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E403-E411.
33. Mills J.H., Thompson L.F., Mueller C., Waickman A.T., Jalkanen S., Niemela J., Airas L., Bynoe M.S. CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9325-9330.
34. Nair A., Frederick T.J., Miller S.D. Astrocytes in multiple sclerosis: a product of their environment. Cell Mol. Life Sci. 2008, 65:2702-2720.
35. Pan W., Banks W.A., Kennedy M.K., Gutierrez E.G., Kastin A.J. Differential permeability of the BBB in acute EAE: enhanced transport of TNF-α. Am. J. Physiol. 1996, 271:E636-E642.
36. Pan W., Hsuchou H., Cornelissen-Guillaume G.G., Jayaram B., Wang Y., Tu H., Halberg F., Wu X., Chua S.C., Kastin A.J. Endothelial leptin receptor mutation provides partial resistance to diet-induced obesity. J. Appl. Physiol. 2012, 112:1410-1418.
37. Pan W., Hsuchou H., He Y., Sakharkar A., Cain C., Yu C., Kastin A.J. Astrocyte leptin receptor (ObR) and leptin transport in adult-onset obese mice. Endocrinology 2008, 149:2798-2806.
38. Pan W., Hsuchou H., Jayaram B., Khan R.S., Huang E.Y.K., Wu X., Chen C., Kastin A.J. Leptin action on non-neuronal cells in the CNS: potential clinical implications. Ann. N.Y. Acad. Sci. 2012, 1264:64-71.
39. vy mice. J. Mol. Neurosci. 2011, 43:478-484.
40. Pan W., Kastin A.J. Adipokines and the blood-brain barrier. Peptides 2007, 28:1317-1330.
41. Pino P.A., Cardona A.E. Isolation of brain and spinal cord mononuclear cells using percoll gradients. J. Vis. Exp. 2011, (48). pii:2348. 10.3791/2348.
42. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 1997, 20:570-577.
43. Sanna V., Di G.A., La C.A., Lechler R.I., Fontana S., Zappacosta S., Matarese G. Leptin surge precedes onset of autoimmune encephalomyelitis and correlates with development of pathogenic T cell responses. J. Clin. Invest. 2003, 111:241-250.
44. Simmons S.B., Pierson E.R., Lee S.Y., Goverman J.M. Modeling the heterogeneity of multiple sclerosis in animals. Trends Immunol. 2013, 34:410-422.
45. Tang B.L. Leptin as a neuroprotective agent. Biochem. Biophys. Res. Commun. 2008, 368:181-185.
46. Tsutsui S., Schnermann J., Noorbakhsh F., Henry S., Yong V.W., Winston B.W., Warren K., Power C. A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J. Neurosci. 2004, 24:1521-1529.
47. Wei W., Du C., Lv J., Zhao G., Li Z., Wu Z., Hasko G., Xie X. Blocking A2B adenosine receptor alleviates pathogenesis of experimental autoimmune encephalomyelitis via inhibition of IL-6 production and Th17 differentiation. J. Immunol. 2013, 190:138-146.
48. Wu X., Mishra P.K., Hsuchou H., Kastin A.J., Pan W. Upregulation of astrocytic leptin receptor in mice with experimental autoimmune encephalomyelitis. J. Mol. Neurosci. 2013, 49:446-456.
49. Wu X., Pan W., He Y., Hsuchou H., Kastin A.J. Cerebral interleukin-15 shows upregulation and beneficial effects in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2010, 223:65-72.
50. Xu L., Rensing N., Yang X.F., Zhang H.X., Thio L.L., Rothman S.M., Weisenfeld A.E., Wong M., Yamada K.A. Leptin inhibits 4-aminopyridine- and pentylenetetrazole-induced seizures and AMPAR-mediated synaptic transmission in rodents. J. Clin. Invest. 2008, 118:272-280.
51. Yi H., Guo C., Yu X., Zuo D., Wang X.Y. Mouse CD11b+Gr-1+ myeloid cells can promote Th17 cell differentiation and experimental autoimmune encephalomyelitis. J. Immunol. 2012, 189:4295-4304.
52. Zamanian J.L., Xu L., Foo L.C., Nouri N., Zhou L., Giffard R.G., Barres B.A. Genomic analysis of reactive astrogliosis. J. Neurosci. 2012, 32:6391-6410.
53. Zehntner S.P., Brickman C., Bourbonniere L., Remington L., Caruso M., Owens T. Neutrophils that infiltrate the central nervous system regulate T cell responses. J. Immunol. 2005, 174:5124-5131.