Mast Cells Release Chemokine CCL2 in Response to Parkinsonian Toxin 1-Methyl-4-Phenyl-Pyridinium (MPP+)

Neurochemical Research

Volumn 41, Issue 5, 2016, Pages 1042-1049

  Kempuraj, Duraisamy ^a,b   Thangavel, Ramasamy ^a,b   Fattal, Ranan ^b   Pattani, Sagar ^b   Yang, Evert ^b   Zaheer, Smita ^b   Santillan, Donna A ^b   Santillan, Mark K ^b   Zaheer, Asgar ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

1 Methyl 4 phenyl pyridinium; CCL2; Glia maturation factor; Mast cells; Parkinson s disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; GLIA MATURATION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 4; SLC25A27 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ARTICLE; ASTROCYTE; BONE MARROW DERIVED MAST CELL; CELL ACTIVATION; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE OVEREXPRESSION; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MAST CELL; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL CORD BLOOD DERIVED CULTURED MAST CELL; ANIMAL; CELL CULTURE; CYTOLOGY; FETUS BLOOD; GENETICS; KNOCKOUT MOUSE; METABOLISM; SECRETION (PROCESS);

1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; ASTROCYTES; CELLS, CULTURED; CHEMOKINE CCL2; COCULTURE TECHNIQUES; FETAL BLOOD; GLIA MATURATION FACTOR; HUMANS; MAST CELLS; MICE; MICE, KNOCKOUT; MITOCHONDRIAL UNCOUPLING PROTEINS; PARKINSON DISEASE;

EID: 84949493464     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-015-1790-z     Document Type: Article

References (58)

1. Dong H, Zhang X, Qian Y (2014) Mast cells and neuroinflammation. Med Sci Monit Basic Res 20:200–206
2. Lyman M, Lloyd DG, Ji X, Vizcaychipi MP, Ma D (2014) Neuroinflammation: the role and consequences. Neurosci Res 79:1–12
3. Jarrott B, Williams SJ (2015) Chronic brain inflammation: the neurochemical basis for drugs to reduce inflammation. Neurochem Res. doi:10.1007/s11064-015-1661-7
4. Trudler D, Nash Y, Frenkel D (2015) New insights on Parkinson’s disease genes: the link between mitochondria impairment and neuroinflammation. J Neural Transm 122:1409–1419
5. Stojkovska I, Wagner BM, Morrison BE (2015) Parkinson’s disease and enhanced inflammatory response. Exp Biol Med (Maywood) 240:1387–1395
6. Czlonkowska A, Kohutnicka M, Kurkowska-Jastrzebska I, Czlonkowski A (1996) Microglial reaction in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) induced Parkinson’s disease mice model. Neurodegeneration 5:137–143
7. +))-induced cell death via the mitochondrial apoptotic pathway. Eur J Pharmacol 713:58–67
8. Khan MM, Kempuraj D, Zaheer S, Zaheer A (2014) Glia maturation factor deficiency suppresses 1-methyl-4-phenylpyridinium-induced oxidative stress in astrocytes. J Mol Neurosci 53:590–599
9. Lim R, Miller JF, Zaheer A (1989) Purification and characterization of glia maturation factor beta: a growth regulator for neurons and glia. Proc Natl Acad Sci USA 86:3901–3905
10. Lim R, Zaheer A (1991) Structure and function of glia maturation factor beta. Adv Exp Med Biol 296:161–164
11. Kaplan R, Zaheer A, Jaye M, Lim R (1991) Molecular cloning and expression of biologically active human glia maturation factor-beta. J Neurochem 57:483–490
12. Zaheer A, Fink BD, Lim R (1993) Expression of glia maturation factor beta mRNA and protein in rat organs and cells. J Neurochem 60:914–920
13. Zaheer S, Wu Y, Sahu SK, Zaheer A (2011) Suppression of neuro inflammation in experimental autoimmune encephalomyelitis by glia maturation factor antibody. Brain Res 1373:230–239
14. Zaheer A, Zaheer S, Sahu SK, Knight S, Khosravi H, Mathur SN, Lim R (2007) A novel role of glia maturation factor: induction of granulocyte–macrophage colony-stimulating factor and pro-inflammatory cytokines. J Neurochem 101:364–376
15. Khan MM, Zaheer S, Thangavel R, Patel M, Kempuraj D, Zaheer A (2015) Absence of Glia maturation factor protects dopaminergic neurons and improves motor behavior in mouse model of parkinsonism. Neurochem Res 40:980–990
16. Zaheer S, Wu Y, Sahu SK, Zaheer A (2010) Overexpression of glia maturation factor reinstates susceptibility to myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis in glia maturation factor deficient mice. Neurobiol Dis 40:593–598
17. Zaheer A, Mathur SN, Lim R (2002) Overexpression of glia maturation factor in astrocytes leads to immune activation of microglia through secretion of granulocyte–macrophage-colony stimulating factor. Biochem Biophys Res Commun 294:238–244
18. Skaper SD, Facci L, Giusti P (2014) Neuroinflammation, microglia and mast cells in the pathophysiology of neurocognitive disorders: a review. CNS Neurol Disord Drug Targets 13:1654–1666
19. Nelissen S, Lemmens E, Geurts N, Kramer P, Maurer M, Hendriks J, Hendrix S (2013) The role of mast cells in neuroinflammation. Acta Neuropathol 125:637–650
20. Skaper SD, Giusti P, Facci L (2012) Microglia and mast cells: two tracks on the road to neuroinflammation. FASEB J 26:3103–3117
21. Kim DY, Jeoung D, Ro JY (2010) Signaling pathways in the activation of mast cells cocultured with astrocytes and colocalization of both cells in experimental allergic encephalomyelitis. J Immunol 185:273–283
22. Kempuraj D, Thangavel R, Yang E, Pattani S, Zaheer S, Santillan DA, Santillan MK, Zaheer A (2015) Dopaminergic toxin 1-methyl-4-phenylpyridinium, proteins alpha-synuclein and Glia maturation factor activate mast cells and release inflammatory mediators. PLoS One 10:e0135776
23. Conti B, Sugama S, Lucero J, Winsky-Sommerer R, Wirz SA, Maher P, Andrews Z, Barr AM, Morale MC, Paneda C, Pemberton J, Gaidarova S, Behrens MM, Beal F, Sanna PP, Horvath T, Bartfai T (2005) Uncoupling protein 2 protects dopaminergic neurons from acute 1,2,3,6-methyl-phenyl-tetrahydropyridine toxicity. J Neurochem 93:493–501
24. Tagen M, Elorza A, Kempuraj D, Boucher W, Kepley CL, Shirihai OS, Theoharides TC (2009) Mitochondrial uncoupling protein 2 inhibits mast cell activation and reduces histamine content. J Immunol 183:6313–6319
25. +-and dopamine-induced oxidative stress, mitochondrial depolarization, and ATP deficiency in neurons and is interlinked with UCP2 expression. Free Radic Biol Med 46:810–820
26. Ho PW, Ho JW, Liu HF, So DH, Tse ZH, Chan KH, Ramsden DB, Ho SL (2012) Mitochondrial neuronal uncoupling proteins: a target for potential disease-modification in Parkinson’s disease. Transl Neurodegener 1:3
27. Lim R, Zaheer A, Khosravi H, Freeman JH Jr, Halverson HE, Wemmie JA, Yang B (2004) Impaired motor performance and learning in glia maturation factor-knockout mice. Brain Res 1024:225–232
28. Kim DY, Hong GU, Ro JY (2011) Signal pathways in astrocytes activated by cross-talk between of astrocytes and mast cells through CD40-CD40L. J Neuroinflammation 8:25
29. Sayed BA, Walker ME, Brown MA (2011) Cutting edge: mast cells regulate disease severity in a relapsing-remitting model of multiple sclerosis. J Immunol 186:3294–3298
30. Zaheer A, Yorek MA, Lim R (2001) Effects of glia maturation factor overexpression in primary astrocytes on MAP kinase activation, transcription factor activation, and neurotrophin secretion. Neurochem Res 26:1293–1299
31. Zaheer A, Yang B, Cao X, Lim R (2004) Decreased copper-zinc superoxide dismutase activity and increased resistance to oxidative stress in glia maturation factor-null astrocytes. Neurochem Res 29:1473–1480
32. Kempuraj D, Khan MM, Thangavel R, Xiong Z, Yang E, Zaheer A (2013) Glia maturation factor induces interleukin-33 release from astrocytes: implications for neurodegenerative diseases. J Neuroimmune Pharmacol 8:643–650
33. Kempuraj D, Saito H, Kaneko A, Fukagawa K, Nakayama M, Toru H, Tomikawa M, Tachimoto H, Ebisawa M, Akasawa A, Miyagi T, Kimura H, Nakajima T, Tsuji K, Nakahata T (1999) Characterization of mast cell-committed progenitors present in human umbilical cord blood. Blood 93:3338–3346
34. Kempuraj D, Asadi S, Zhang B, Manola A, Hogan J, Peterson E, Theoharides TC (2010) Mercury induces inflammatory mediator release from human mast cells. J Neuroinflammation 7:20
35. Santillan MK, Leslie KK, Hamilton WS, Boese BJ, Ahuja M, Hunter SK, Santillan DA (2014) Collection of a lifetime: a practical approach to developing a longitudinal collection of women’s healthcare biological samples. Eur J Obstet Gynecol Reprod Biol 179:94–99
36. Bulfone-Paus S, Bahri R (2015) Mast cells as regulators of T cell responses. Front Immunol 6:394
37. Theoharides TC, Valent P, Akin C (2015) Mast cells, mastocytosis, and related disorders. N Engl J Med 373:163–172
38. Theoharides TC, Alysandratos KD, Angelidou A, Delivanis DA, Sismanopoulos N, Zhang B, Asadi S, Vasiadi M, Weng Z, Miniati A, Kalogeromitros D (2012) Mast cells and inflammation. Biochim Biophys Acta 1822:21–33
39. Silver R, Curley JP (2013) Mast cells on the mind: new insights and opportunities. Trends Neurosci 36:513–521
40. Chikahisa S, Kodama T, Soya A, Sagawa Y, Ishimaru Y, Sei H, Nishino S (2013) Histamine from brain resident MAST cells promotes wakefulness and modulates behavioral states. PLoS One 8:e78434
41. Skaper SD, Facci L, Barbierato M, Zusso M, Bruschetta G, Impellizzeri D, Cuzzocrea S, Giusti P (2015) N-Palmitoylethanolamine and neuroinflammation: a novel therapeutic strategy of resolution. Mol Neurobiol 52:1034–1042
42. Kalesnikoff J, Galli SJ (2008) New developments in mast cell biology. Nat Immunol 9:1215–1223
43. Mekori YA, Metcalfe DD (2000) Mast cells in innate immunity. Immunol Rev 173:131–140
44. Sismanopoulos N, Delivanis DA, Alysandratos KD, Angelidou A, Therianou A, Kalogeromitros D, Theoharides TC (2012) Mast cells in allergic and inflammatory diseases. Curr Pharm Des 18:2261–2277
45. Madrigal JL, Caso JR (2014) The chemokine (C-C motif) ligand 2 in neuroinflammation and neurodegeneration. Adv Exp Med Biol 824:209–219
46. Stamatovic SM, Shakui P, Keep RF, Moore BB, Kunkel SL, Van Rooijen N, Andjelkovic AV (2005) Monocyte chemoattractant protein-1 regulation of blood–brain barrier permeability. J Cereb Blood Flow Metab 25:593–606
47. Yao Y, Tsirka SE (2014) Monocyte chemoattractant protein-1 and the blood–brain barrier. Cell Mol Life Sci 71:683–697
48. Reale M, Iarlori C, Thomas A, Gambi D, Perfetti B, Di Nicola M, Onofrj M (2009) Peripheral cytokines profile in Parkinson’s disease. Brain Behav Immun 23:55–63
49. Thangavel R, Stolmeier D, Yang X, Anantharam P, Zaheer A (2012) Expression of glia maturation factor in neuropathological lesions of Alzheimer’s disease. Neuropathol Appl Neurobiol 38:572–581
50. Zaheer S, Thangavel R, Sahu SK, Zaheer A (2011) Augmented expression of glia maturation factor in Alzheimer’s disease. Neuroscience 194:227–233
51. Zaheer A, Knight S, Zaheer A, Ahrens M, Sahu SK, Yang B (2008) Glia maturation factor overexpression in neuroblastoma cells activates glycogen synthase kinase-3beta and caspase-3. Brain Res 1190:206–214
52. Zaheer A, Zaheer S, Thangavel R, Wu Y, Sahu SK, Yang B (2008) Glia maturation factor modulates beta-amyloid-induced glial activation, inflammatory cytokine/chemokine production and neuronal damage. Brain Res 1208:192–203
53. +))-induced loss of mesencephalic dopaminergic neurons. Neuroscience 277:196–205
54. Reddy PH, Reddy TP (2011) Mitochondria as a therapeutic target for aging and neurodegenerative diseases. Curr Alzheimer Res 8:393–409
55. Andrews ZB, Horvath B, Barnstable CJ, Elsworth J, Yang L, Beal MF, Roth RH, Matthews RT, Horvath TL (2005) Uncoupling protein-2 is critical for nigral dopamine cell survival in a mouse model of Parkinson’s disease. J Neurosci 25:184–191
56. Ramsden DB, Ho PW, Ho JW, Liu HF, So DH, Tse HM, Chan KH, Ho SL (2012) Human neuronal uncoupling proteins 4 and 5 (UCP4 and UCP5): structural properties, regulation, and physiological role in protection against oxidative stress and mitochondrial dysfunction. Brain Behav 2:468–478
57. Negre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Penicaud L, Casteilla L (1997) A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11:809–815
58. Rousset S, Emre Y, Join-Lambert O, Hurtaud C, Ricquier D, Cassard-Doulcier AM (2006) The uncoupling protein 2 modulates the cytokine balance in innate immunity. Cytokine 35:135–142