Inhibition of store-operated calcium entry in microglia by helminth factors: Implications for immune suppression in neurocysticercosis

Journal of Neuroinflammation

Volumn 11, Issue 1, 2014, Pages

  Sun, Yuyang ^a   Chauhan, Arun ^a   Sukumaran, Pramod ^a   Sharma, Jyotika ^a   Singh, Brij B ^a   Mishra, Bibhuti B ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Calcium signaling; Helminth; Immune suppression; Microglia; Neurocysticercosis; Neuroinflammation; ORAI1; Store operated calcium entry; TRPC1

Indexed keywords

CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; HELMINTH PROTEIN; HELMINTH SOLUBLE FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; STRESS ACTIVATED PROTEIN KINASE; STROMAL INTERACTION MOLECULE 1; THAPSIGARGIN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR RELA; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; UNCLASSIFIED DRUG; CALCIUM CHANNEL;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENDOPLASMIC RETICULUM; FEMALE; HELMINTH; IMMUNOPRECIPITATION; INNATE IMMUNITY; MESOCESTOIDES CORTI; MICROGLIA; MOUSE; NEUROCYSTICERCOSIS; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STORE OPERATED CALCIUM ENTRY; UPREGULATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PATCH CLAMP TECHNIQUE;

ANIMALS; BLOTTING, WESTERN; CALCIUM CHANNELS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; IMMUNE TOLERANCE; IMMUNOPRECIPITATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROGLIA; NEUROCYSTICERCOSIS; PATCH-CLAMP TECHNIQUES;

EID: 84924914968     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-014-0210-7     Document Type: Article

References (82)

1. Nash TE, Singh G, White AC, Rajshekhar V, Loeb JA, Proaño JV, Takayanagui OM, Gonzalez AE, Butman JA, DeGiorgio C, Del Brutto OH, Delgado-Escueta A, Evans CA, Gilman RH, Martinez SM, Medina MT, Pretell EJ, Teale J, Garcia HH: Treatment of neurocysticercosis: current status and future research needs. Neurology 2006, 67:1120-1127.
2. White AC Jr: Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Annu Rev Med 2000, 51:187-206.
3. White AC Jr: Neurocysticercosis: a major cause of neurological disease worldwide. Clin Infect Dis 1997, 24:101-115.
4. Robinson P, Atmar RL, Lewis DE, White AC Jr: Granuloma cytokines in murine cysticercosis. Infect Immun 1997, 65:2925-2931.
5. Restrepo BI, Alvarez JI, Castaño JA, Arias LF, Restrepo M, Trujillo J, Colegial CH, Teale JM: Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infect Immun 2001, 69:4554-4560.
6. White AC Jr, Robinson P, Kuhn R: Taenia solium cysticercosis: host-parasite interactions and the immune response. Chem Immunol 1997, 66:209-230.
7. Rivest S: Regulation of innate immune responses in the brain. Nat Rev Immunol 2009, 9:429-439.
8. Takeda K, Kaisho T, Akira S: Toll-like receptors. Annu Rev Immunol 2003, 21:335-376.
9. Dabbagh K, Lewis DB: Toll-like receptors and T-helper-1/T-helper-2 responses. Curr Opin Infect Dis 2003, 16:199-204.
10. Cherry JD, Olschowka JA, O'Banion MK: Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation 2014, 11:98.
11. Geijtenbeek TB, van Vliet SJ, Engering A, 't Hart BA, van Kooyk Y: Self- and nonself-recognition by C-type lectins on dendritic cells. Annu Rev Immunol 2004, 22:33-54.
12. Medzhitov R: Toll-like receptors and innate immunity. Nat Rev Immunol 2001, 1:135-145.
13. Banchereau J, Steinman RM: Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
14. Mishra BB, Gundra UM, Wong K, Teale JM: MyD88-deficient mice exhibit decreased parasite-induced immune responses but reduced disease severity in a murine model of neurocysticercosis. Infect Immun 2009, 77:5369-5379.
15. 2+ signaling just got STIMy: an update on STIM1 activated TRPC channels. Front Biosci 2012, 17:805-823.
16. Putney JW Jr, Broad LM, Braun FJ, Lievremont JP, Bird GS: Mechanisms of capacitative calcium entry. J Cell Sci 2001, 114:2223-2229.
17. Alvarez JI, Mishra BB, Gundra UM, Mishra PK, Teale JM: Mesocestoides corti intracranial infection as a murine model for neurocysticercosis. Parasitology 2010, 137:359-372.
18. Floden AM, Li S, Combs CK: β-amyloid-stimulated microglia induce neuron death via synergistic stimulation of tumor necrosis factor α and NMDA receptors. J Neurosci 2005, 25:2566-2575.
19. Nagamoto-Combs K, Combs CK: Microglial phenotype is regulated by activity of the transcription factor, NFAT (nuclear factor of activated T cells). J Neurosci 2010, 30:9641-9646.
20. -/- mice. Proc Natl Acad Sci U S A 2007, 104:17542-17547.
21. 2+ ATPase 2 gene silencing promotes cell survival: a potential role for TRPC1 in Darier's disease. Mol Biol Cell 2006, 17:4446-4458.
22. Singh BB, Zheng C, Liu X, Lockwich T, Liao D, Zhu MX, Birnbaumer L, Ambudkar IS: Trp1-dependent enhancement of salivary gland fluid secretion: role of store-operated calcium entry. FASEB J 2001, 15:1652-1654.
23. 2+ entry (SOCE). J Biol Chem 2008, 283:17333-17340.
24. Pani B, Ong HL, Brazer SC, Liu X, Rauser K, Singh BB, Ambudkar IS: Activation of TRPC1 by STIM1 in ER-PM microdomains involves release of the channel from its scaffold caveolin-1. Proc Natl Acad Sci U S A 2009, 106:20087-20092.
25. Pani B, Liu X, Bollimuntha S, Cheng KT, Niesman IR, Zheng C, Achen VR, Patel HH, Ambudkar IS, Singh BB: Impairment of TRPC1-STIM1 channel assembly and AQP5 translocation compromise agonist-stimulated fluid secretion in mice lacking caveolin1. J Cell Sci 2013, 126:667-675.
26. Mishra BB, Gundra UM, Teale JM: Toll-like receptors in CNS parasitic infections. Curr Top Microbiol Immunol 2009, 336:83-104.
27. Palm NW, Medzhitov R: Pattern recognition receptors and control of adaptive immunity. Immunol Rev 2009, 227:221-233.
28. Izquierdo JH, Bonilla-Abadía F, Cañas CA, Tobón GJ: Calcium, channels, intracellular signaling and autoimmunity. Reumatol Clin 2014, 10:43-47.
29. Feske S: Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol 2007, 7:690-702.
30. Debnath M, Venkatasubramanian G: Recent advances in psychoneuroimmunology relevant to schizophrenia therapeutics. Curr Opin Psychiatry 2013, 26:433-439.
31. Morales I, Guzmán-Martínez L, Cerda-Troncoso C, Farías GA, Maccioni RB: Neuroinflammation in the pathogenesis of Alzheimer's disease: a rational framework for the search of novel therapeutic approaches. Front Cell Neurosci 2014, 8:112.
32. Amor S, Puentes F, Baker D, van der Valk P: Inflammation in neurodegenerative diseases. Immunology 2010, 129:154-169.
33. Hewitson JP, Grainger JR, Maizels RM: Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009, 167:1-11.
34. Ransohoff RM, Kivisäkk P, Kidd G: Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003, 3:569-581.
35. Chavarria A, Alcocer-Varela J: Is damage in central nervous system due to inflammation? Autoimmun Rev 2004, 3:251-260.
36. Ransohoff RM, Liu L, Cardona AE: Chemokines and chemokine receptors: multipurpose players in neuroinflammation. Int Rev Neurobiol 2007, 82:187-204.
37. Nguyen MD, Julien JP, Rivest S: Innate immunity: the missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci 2002, 3:216-227.
38. Qian L, Flood PM, Hong JS: Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J Neural Transm 2010, 117:971-979.
39. Lull ME, Block ML: Microglial activation and chronic neurodegeneration. Neurotherapeutics 2010, 7:354-365.
40. McGeer PL, McGeer EG: Glial reactions in Parkinson's disease. Mov Disord 2008, 23:474-483.
41. Orr CF, Rowe DB, Halliday GM: An inflammatory review of Parkinson's disease. Prog Neurobiol 2002, 68:325-340.
42. Block ML, Hong JS: Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 2005, 76:77-98.
43. Kielian T, Esen N, Bearden ED: Toll-like receptor 2 (TLR2) is pivotal for recognition of S. aureus peptidoglycan but not intact bacteria by microglia. Glia 2005, 49:567-576.
44. Koedel U, Rupprecht T, Angele B, Heesemann J, Wagner H, Pfister HW, Kirschning CJ: MyD88 is required for mounting a robust host immune response to Streptococcus pneumoniae in the CNS. Brain 2004, 127:1437-1445.
45. Turrin NP, Rivest S: Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy. Neurobiol Dis 2004, 16:321-334.
46. Mishra BB, Mishra PK, Teale JM: Expression and distribution of Toll-like receptors in the brain during murine neurocysticercosis. J Neuroimmunol 2006, 181:46-56.
47. Cummings RD, Nyame AK: Glycobiology of schistosomiasis. FASEB J 1996, 10:838-848.
48. Khoo KH, Dell A: Glycoconjugates from parasitic helminths: structure diversity and immunobiological implications. Adv Exp Med Biol 2001, 491:185-205.
49. Alvarez JI, Rivera J, Teale JM: Differential release and phagocytosis of tegument glycoconjugates in neurocysticercosis: implications for immune evasion strategies. PLoS Negl Trop Dis 2008, 2:e218.
50. Sciutto E, Chavarria A, Fragoso G, Fleury A, Larralde C: The immune response in Taenia solium cysticercosis: protection and injury. Parasite Immunol 2007, 29:621-636.
51. Tsang VC, Brand JA, Boyer AE: An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis 1989, 159:50-59.
52. Restrepo BI, Obregón-Henao A, Mesa M, Gil DL, Ortiz BL, Mejía JS, Villota GE, Sanzón F, Teale JM: Characterisation of the carbohydrate components of Taenia solium metacestode glycoprotein antigens. Int J Parasitol 2000, 30:689-696.
53. Haslam SM, Restrepo BI, Obregón-Henao A, Teale JM, Morris HR, Dell A: Structural characterization of the N-linked glycans from Taenia solium metacestodes. Mol Biochem Parasitol 2003, 126:103-107.
54. Correa D, Dalma D, Espinoza B, Plancarte A, Rabiela MT, Madrazo I, Gorodezky C, Flisser A: Heterogeneity of humoral immune components in human cysticercosis. J Parasitol 1985, 71:535-541.
55. Grewal JS, Kaur S, Bhatti G, Sawhney IM, Ganguly NK, Mahajan RC, Malla N: Cellular immune responses in human neurocysticercosis. Parasitol Res 2000, 86:500-503.
56. Bafica A, Santiago HC, Goldszmid R, Ropert C, Gazzinelli RT, Sher A: Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol 2006, 177:3515-3519.
57. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, Halmen KA, Lamphier M, Olivier M, Bartholomeu DC, Gazzinelli RT, Golenbock DT: Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U S A 2007, 104:1919-1924.
58. Hernández M, Gonzalez LM, Fleury A, Saenz B, Parkhouse RM, Harrison LJ, Garate T, Sciutto E: Neurocysticercosis: detection of Taenia solium DNA in human cerebrospinal fluid using a semi-nested PCR based on HDP2. Ann Trop Med Parasitol 2008, 102:317-323.
59. Almeida CR, Ojopi EP, Nunes CM, Machado LR, Takayanagui OM, Livramento JA, Abraham R, Gattaz WF, Vaz AJ, Dias-Neto E: Taenia solium DNA is present in the cerebrospinal fluid of neurocysticercosis patients and can be used for diagnosis. Eur Arch Psychiatry Clin Neurosci 2006, 256:307-310.
60. Farber K, Kettenmann H: Functional role of calcium signals for microglial function. Glia 2006, 54:656-665.
61. Sun Y, Sukumaran P, Bandyopadhyay BC, Singh BB: Physiological function and characterization of TRPCs in neurons. Cells 2014, 3:455-475.
62. Parekh AB, Putney JW Jr: Store-operated calcium channels. Physiol Rev 2005, 85:757-810.
63. 2+ entry in rat microglia. Channels (Austin) 2009, 3:129-139.
64. Muik M, Frischauf I, Derler I, Fahrner M, Bergsmann J, Eder P, Schindl R, Hesch C, Polzinger B, Fritsch R, Kahr H, Madl J, Gruber H, Groschner K, Romanin C: Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem 2008, 283:8014-8022.
65. Navarro-Borelly L, Somasundaram A, Yamashita M, Ren D, Miller RJ, Prakriya M: STIM1-Orai1 interactions and Orai1 conformational changes revealed by live-cell FRET microscopy. J Physiol 2008, 586:5383-5401.
66. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 2006, 174:803-813.
67. Liou J, Fivaz M, Inoue T, Meyer T: Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. Proc Natl Acad Sci U S A 2007, 104:9301-9306.
68. Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS: STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009, 136:876-890.
69. Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS: Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 2008, 454:538-542.
70. Ong HL, Cheng KT, Liu X, Bandyopadhyay BC, Paria BC, Soboloff J, Pani B, Gwack Y, Srikanth S, Singh BB, Gill DL, Ambudkar IS: Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx: evidence for similarities in store-operated and calcium release-activated calcium channel components. J Biol Chem 2007, 282:9105-9116.
71. Chano F, Descoteaux A: Modulation of lipopolysaccharide-induced NF-IL6 activation by protein kinase C-α in a mouse macrophage cell line. Eur J Immunol 2002, 32:2897-2904.
72. Chen BC, Hsieh SL, Lin WW: Involvement of protein kinases in the potentiation of lipopolysaccharide-induced inflammatory mediator formation by thapsigargin in peritoneal macrophages. J Leukoc Biol 2001, 69:280-288.
73. Chen CC, Wang JK, Lin SB: Antisense oligonucleotides targeting protein kinase C-α, -βI, or -δ but not -η inhibit lipopolysaccharide-induced nitric oxide synthase expression in RAW 264.7 macrophages: involvement of a nuclear factor κΒ-dependent mechanism. J Immunol 1998, 161:6206-6214.
74. Fujihara M, Connolly N, Ito N, Suzuki T: Properties of protein kinase C isoforms (βII, ε, and ζ) in a macrophage cell line (J774) and their roles in LPS-induced nitric oxide production. J Immunol 1994, 152:1898-1906.
75. Giroux M, Descoteaux A: Cyclooxygenase-2 expression in macrophages: modulation by protein kinase C-α. J Immunol 2000, 165:3985-3991.
76. Goodridge HS, Harnett W, Liew FY, Harnett MM: Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and -independent mechanisms and the implications for bioactive IL-12 and IL-23 responses. Immunology 2003, 109:415-425.
77. Kontny E, Kurowska M, Szczepańska K, Maśliński W: Rottlerin, a PKC isozyme-selective inhibitor, affects signaling events and cytokine production in human monocytes. J Leukoc Biol 2000, 67:249-258.
78. Novotney M, Chang ZL, Uchiyama H, Suzuki T: Protein kinase C in tumoricidal activation of mouse macrophage cell lines. Biochemistry 1991, 30:5597-5604.
79. Shinji H, Akagawa KS, Tsuji M, Maeda M, Yamada R, Matsuura K, Yamamoto S, Yoshida T: Lipopolysaccharide-induced biphasic inositol 1,4,5-trisphosphate response and tyrosine phosphorylation of 140-kilodalton protein in mouse peritoneal macrophages. J Immunol 1997, 158:1370-1376.
80. St-Denis A, Chano F, Tremblay P, St-Pierre Y, Descoteaux A: Protein kinase C-α modulates lipopolysaccharide-induced functions in a murine macrophage cell line. J Biol Chem 1998, 273:32787-32792.
81. Langlet C, Springael C, Johnson J, Thomas S, Flamand V, Leitges M, Goldman M, Aksoy E, Willems F: PKC-α controls MYD88-dependent TLR/IL-1R signaling and cytokine production in mouse and human dendritic cells. Eur J Immunol 2010, 40:505-515.
82. Pozo-Guisado E, Campbell DG, Deak M, Alvarez-Barrientos A, Morrice NA, Alvarez IS, Alessi DR, Martín-Romero FJ: Phosphorylation of STIM1 at ERK1/2 target sites modulates store-operated calcium entry. J Cell Sci 2010, 123:3084-3093.