STIM1, STIM2, and orai1 regulate store-operated calcium entry and purinergic activation of microglia

GLIA

Volumn 63, Issue 4, 2015, Pages 652-663

  Michaelis, Marlen ^a   Nieswandt, Bernhard ^b   Stegner, David ^b   Eilers, Jens ^a   Kraft, Robert ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Microglia; Migration; Phagocytosis; Store operated calcium entry

Indexed keywords

2 METHYLTHIOADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CYCLOPIAZONIC ACID; LIPOPOLYSACCHARIDE; NUCLEOTIDE; PURINERGIC P2Y6 RECEPTOR AGONIST; PURINERGIC RECEPTOR STIMULATING AGENT; STROMAL INTERACTION MOLECULE 1; STROMAL INTERACTION MOLECULE 2; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; ADENOSINE DIPHOSPHATE; CALCIUM; CALCIUM CHANNEL; INDOLE DERIVATIVE; LIPOPOLYSACCHARIDE A; MEMBRANE PROTEIN; METHYLTHIO-ADP; ORAI1 PROTEIN, MOUSE; STIM1 PROTEIN, MOUSE; STIM2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL ACTIVATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; INFLAMMATION; MALE; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STORE OPERATED CALCIUM ENTRY; ANALOGS AND DERIVATIVES; ANIMAL; CALCIUM SIGNALING; CULTURE TECHNIQUE; CYTOLOGY; DEFICIENCY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; TRANSGENIC MOUSE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL CULTURE TECHNIQUES; INDOLES; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROGLIA; PHAGOCYTOSIS; THIONUCLEOTIDES; URIDINE DIPHOSPHATE;

EID: 84922946155     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22775     Document Type: Article

References (54)

1. Abbracchio MP, Burnstock G, Boeynaems J-M, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA. 2006. International union of pharmacology LVIII: Update on the P2Y G protein-coupled nucleotide receptors: From molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58:281-341.
2. Aguzzi A, Barres BA, Bennett ML. 2013. Microglia: Scapegoat, saboteur, or something else? Science 339:156-161.
3. Baba Y, Nishida K, Fujii Y, Hirano T, Hikida M, Kurosaki T. 2008. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat Immunol 9:81-88.
4. Beck A, Penner R, Fleig A. 2008. Lipopolysaccharide-induced down-regulation of Ca2+ release-activated Ca2+ currents (I CRAC) but not Ca2+-activated TRPM4-like currents (I CAN) in cultured mouse microglial cells. J Physiol 586:427-439.
5. Berna-Erro A, Braun A, Kraft R, Kleinschnitz C, Schuhmann MK, Stegner D, Wultsch T, Eilers J, Meuth SG, Stoll G, Nieswandt B. 2009. STIM2 regulates capacitive Ca2+ entry in neurons and plays a key role in hypoxic neuronal cell death. Sci Signal 2:ra67.
6. Brandman O, Liou J, Park WS, Meyer T. 2007. STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:1327-1339.
7. Braun A, Gessner JE, Varga-Szabo D, Syed SN, Konrad S, Stegner D, Vögtle T, Schmidt RE, Nieswandt B. 2009a. STIM1 is essential for Fcγ receptor activation and autoimmune inflammation. Blood 113:1097-1104.
8. Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Bösl M, Stoll G, Nieswandt B. 2009b. Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 113:2056-2063.
9. Cain RJ, Ridley AJ. 2009. Phosphoinositide 3-kinases in cell migration. Biol Cell 101:13-29.
10. Chhatriwala M, Ravi RG, Patel RI, Boyer JL, Jacobson KA, Harden TK. 2004. Induction of novel agonist selectivity for the ADP-activated P2Y1 receptor versus the ADP-activated P2Y12 and P2Y13 receptors by conformational constraint of an ADP analog. J Pharmacol Exp Ther 311:1038-1043.
11. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan W-B. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758.
12. De Simone R, Niturad CE, De Nuccio C, Ajmone-Cat MA, Visentin S, Minghetti L. 2010. TGF-β and LPS modulate ADP-induced migration of microglial cells through P2Y1 and P2Y12 receptor expression. J Neurochem 115:450-459.
13. Ferrari D, Villalba M, Chiozzi P, Falzoni S, Ricciardi-Castagnoli P, Virgilio FD. 1996. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 156:1531-1539.
14. Fumagalli M, Brambilla R, D'Ambrosi N, Volonté C, Matteoli M, Verderio C, Abbracchio MP. 2003. Nucleotide-mediated calcium signaling in rat cortical astrocytes: Role of P2X and P2Y receptors. Glia 43:218-230.
15. Gandhirajan RK, Meng S, Chandramoorthy HC, Mallilankaraman K, Mancarella S, Gao H, Razmpour R, Yang X-F, Houser SR, Chen J, Koch WJ, Wang H, Soboloff J, Gill DL, Madesh M. 2013. Blockade of NOX2 and STIM1 signaling limits lipopolysaccharide-induced vascular inflammation. J Clin Invest 123:887-902.
16. Gitik M, Reichert F, Rotshenker S. 2010. Cytoskeleton plays a dual role of activation and inhibition in myelin and zymosan phagocytosis by microglia. FASEB J 24:2211-2221.
17. Hanisch U-K, Kettenmann H. 2007. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
18. Harteneck C, Frenzel H, Kraft R. 2007. N-(p-amylcinnamoyl)anthranilic acid (ACA): a phospholipase A(2) inhibitor and TRP channel blocker. Cardiovasc Drug Rev 25:61-75.
19. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan W-B, Julius D. 2006. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9:1512-1519.
20. Hiramoto R, Bernecky J, Jurand J, Hamlin M. 1964. The effect of hydrogen ion concentration on fluorescent labelled antibodies. J Histochem Cytochem 12:271-274.
21. Hoffmann A, Kann O, Ohlemeyer C, Hanisch U-K, Kettenmann H. 2003. Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J Neurosci 23:4410-4419.
22. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. 2001. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21:1975-1982.
23. Irino Y, Nakamura Y, Inoue K, Kohsaka S, Ohsawa K. 2008. Akt activation is involved in P2Y12 receptor-mediated chemotaxis of microglia. J Neurosci Res 86:1511-1519.
24. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. 2000. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106-4114.
25. Kar P, Bakowski D, Capite JD, Nelson C, Parekh AB. 2012. Different agonists recruit different stromal interaction molecule proteins to support cytoplasmic Ca2+ oscillations and gene expression. Proc Natl Acad Sci U S A 109:6969-6974.
26. Koenigsknecht-Talboo J, Landreth GE. 2005. Microglial phagocytosis induced by fibrillar β-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 25:8240-8249.
27. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, Joshi BV, Jacobson KA, Kohsaka S, Inoue K. 2007. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446:1091-1095.
28. Kraft R, Grimm C, Grosse K, Hoffmann A, Sauerbruch S, Kettenmann H, Schultz G, Harteneck C. 2004. Hydrogen peroxide and ADP-ribose induce TRPM2-mediated calcium influx and cation currents in microglia. Am J Physiol Cell Physiol 286:C129-C137.
29. Liou J, Kim ML, Do Heo W, Jones JT, Myers JW, Ferrell Jr . JE, Meyer T. 2005. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235-1241.
30. Lis A, Peinelt C, Beck A, Parvez S, Monteilh-Zoller M, Fleig A, Penner R. 2007. CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Curr Biol 17:794-800.
31. Mercer JC, DeHaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney JW. 2006. Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem 281:24979-24990.
32. Möller T, Nolte C, Burger R, Verkhratsky A, Kettenmann H. 1997. Mechanisms of C5a and C3a complement fragment-induced [Ca2+]i signaling in mouse microglia. J Neurosci 17:615-624.
33. 2+ hotspots that boost phagocytosis. Curr Biol 22:1990-1997.
34. Ödemis V, Lipfert J, Kraft R, Hajek P, Abraham G, Hattermann K, Mentlein R, Engele J. 2012. The presumed atypical chemokine receptor CXCR7 signals through Gi/o proteins in primary rodent astrocytes and human glioma cells. Glia 60:372-381.
35. Oh-Hora M, Yamashita M, Hogan PG, Sharma S, Lamperti E, Chung W, Prakriya M, Feske S, Rao A. 2008. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat Immunol 9:432-443.
36. Ohsawa K, Irino Y, Nakamura Y, Akazawa C, Inoue K, Kohsaka S. 2007. Involvement of P2X4 and P2Y12 receptors in ATP-induced microglial chemotaxis. Glia 55:604-616.
37. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT. 2011. Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458.
38. Parekh AB, Penner R. 1997. Store depletion and calcium influx. Physiol Rev 77:901-930.
39. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. 2006. Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230-233.
40. Putney JW Jr. 1986. A model for receptor-regulated calcium entry. Cell Calcium 7:1-12.
41. Ransohoff RM, Perry VH. 2009. Microglial Physiology: Unique stimuli, specialized responses. Ann Rev Immunol 27:119-145.
42. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Veliçelebi G, Stauderman KA. 2005. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435-445.
43. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B. 2012. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691-705.
44. Shah VB, Huang Y, Keshwara R, Ozment-Skelton T, Williams DL, Keshvara L. 2008. β-Glucan activates microglia without inducing cytokine production in dectin-1-dependent manner. J Immunol 180:2777-2785.
45. Stiber J, Hawkins A, Zhang Z-S, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenberg P. 2008. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688-697.
46. Swanson JA. 2008. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Bio 9:639-649.
47. Thiel M, Lis A, Penner R. 2013. STIM2 drives Ca2+ oscillations through store-operated Ca2+ entry caused by mild store depletion. J Physiol 591:1433-1445.
48. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. 2003. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778-783.
49. Uesugi A, Kataoka A, Tozaki-Saitoh H, Koga Y, Tsuda M, Robaye B, Boeynaems J-M, Inoue K. 2012. Involvement of protein kinase D in uridine diphosphate-induced microglial macropinocytosis and phagocytosis. Glia 60:1094-1105.
50. Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, Renné T, Stoll G, Nieswandt B. 2008. The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 205:1583-1591.
51. Yang C, Mo X, Lv J, Liu X, Yuan M, Dong M, Li L, Luo X, Fan X, Jin Z, Liu Z, Liu J. 2012. Lipopolysaccharide enhances FcεRI-mediated mast cell degranulation by increasing Ca2+ entry through store-operated Ca2+ channels: Implications for lipopolysaccharide exacerbating allergic asthma. Exp Physiol 97:1315-1327.
52. Yang S, Zhang JJ, Huang X-Y. 2009. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 15:124-134.
53. Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD. 2006. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443:226-229.
54. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD. 2005. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902-905.