Regulation of a TRPM7-like Current in Rat Brain Microglia

Non-excitable cells use Ca2+ influx for essential functions but usually lack voltage-gated Ca2+ channels. The main routes of Ca2+ entry appear to be store-operated channels or Ca2+-permeable non-selective cation channels, of which the magnesium-inhibited cation (or magnesium-nucleotide-regulated metal cation) current has received considerable recent attention. This current appears to be produced by one of the recently cloned transient receptor potential (TRP) channels, TRPM7. In this study of rat microglia, we identified TRPM7 transcripts and a prevalent current with the hallmark biophysical and pharmacological features of TRPM7. This is the first identification of a TRPM7-like current in the brain. There is little known about how members of the TRPM sub-family normally become activated. Using whole-cell patch clamp recordings from rat microglia, we found that the TRPM7-like current activates spontaneously after break-in and that the current and its activation are inhibited by elevated intracellular Mg2+ but not affected by cell swelling or a wide range of intracellular Ca2+ concentrations. The TRPM7-like current in microglia appears to depend on tyrosine phosphorylation. It was inhibited by several tyrosine kinase inhibitors, including a peptide (Src 40–58) that was shown previously to inhibit Src actions, but not by inactive drugs or peptide analogues. The current did not depend on the cell activation state; i.e. it was the same in microglia recently removed from the brain or when cultured under a wide range of conditions that favor the resting or activated state. Because TRPM7 channels are permeable to Ca2+, this current may be important for microglia functions that depend on elevations in intracellular Ca2+. Non-excitable cells use Ca2+ influx for essential functions but usually lack voltage-gated Ca2+ channels. The main routes of Ca2+ entry appear to be store-operated channels or Ca2+-permeable non-selective cation channels, of which the magnesium-inhibited cation (or magnesium-nucleotide-regulated metal cation) current has received considerable recent attention. This current appears to be produced by one of the recently cloned transient receptor potential (TRP) channels, TRPM7. In this study of rat microglia, we identified TRPM7 transcripts and a prevalent current with the hallmark biophysical and pharmacological features of TRPM7. This is the first identification of a TRPM7-like current in the brain. There is little known about how members of the TRPM sub-family normally become activated. Using whole-cell patch clamp recordings from rat microglia, we found that the TRPM7-like current activates spontaneously after break-in and that the current and its activation are inhibited by elevated intracellular Mg2+ but not affected by cell swelling or a wide range of intracellular Ca2+ concentrations. The TRPM7-like current in microglia appears to depend on tyrosine phosphorylation. It was inhibited by several tyrosine kinase inhibitors, including a peptide (Src 40–58) that was shown previously to inhibit Src actions, but not by inactive drugs or peptide analogues. The current did not depend on the cell activation state; i.e. it was the same in microglia recently removed from the brain or when cultured under a wide range of conditions that favor the resting or activated state. Because TRPM7 channels are permeable to Ca2+, this current may be important for microglia functions that depend on elevations in intracellular Ca2+. Non-excitable cells use trans-membrane Ca2+ influxes for essential cell functions, including proliferation, apoptosis, secretion, volume regulation, and ion homeostasis. Immune cells were among the first and remain among the most intensively studied, with focus on general and more specific roles of Ca2+ signaling, such as mitogenic activation, secretion of lymphokines, cytokines, cytotoxic molecules, and antibodies, and on phagocytosis, respiratory burst, and migration. In parallel, there have been an increasing number of studies on the pathways of Ca2+ entry into these cells. In almost all cases, the role of membrane potential in Ca2+ influx in non-excitable cells is fundamentally different from excitable cells. Voltage-gated Ca2+ channels are rare in immune cells, and many cell types appear to be devoid of them. In these cells, although Ca2+ influx is electrogenic and tends to depolarize the cell, the main effect of depolarization is to reduce the driving force for Ca2+ influx. Because hyperpolarization favors Ca2+ entry, the focus has been on store-operated Ca2+ channels, including the Ca2+-release-activated Ca2+ (CRAC) 1The abbreviations used are: CRAC, Ca2+-release-activated Ca2+; ACM, astrocyte conditioned medium; 2-APB, 2-aminoethyldiphenyl borate; K4BAPTA, K41,2-bis(2-aminophenoxy) ethane N,N,N′,N′-tetraacetic acid; MEM, minimal essential medium; nMDG, n-methyl d-glucamine; NPPB, 5-nitro-2-(3-phenylpropylamino)benzoic acid; TRP, transient receptor potential; PLC, phospholipase C.1The abbreviations used are: CRAC, Ca2+-release-activated Ca2+; ACM, astrocyte conditioned medium; 2-APB, 2-aminoethyldiphenyl borate; K4BAPTA, K41,2-bis(2-aminophenoxy) ethane N,N,N′,N′-tetraacetic acid; MEM, minimal essential medium; nMDG, n-methyl d-glucamine; NPPB, 5-nitro-2-(3-phenylpropylamino)benzoic acid; TRP, transient receptor potential; PLC, phospholipase C. channel, and on Ca2+-permeable non-selective cation channels. The CRAC current is widely expressed in immune cells, where it is one of the best characterized store-operated channels (1Parekh A.B. Penner R. Physiol. Rev. 1997; 77: 901-930Crossref PubMed Scopus (1287) Google Scholar, 2Lewis R.S. Adv. Second Messenger Phosphoprotein Res. 1999; 33: 279-307Crossref PubMed Scopus (83) Google Scholar). However, two Ca2+-permeable channel types studies on the cell and rat cells were the first to CRAC and a cation current metal cation Penner R. Physiol. PubMed Scopus Google Scholar, Physiol. PubMed Scopus Google Scholar, R.S. Physiol. PubMed Scopus Google Scholar). The current is to one of the recently cloned transient receptor potential (TRP) channels, TRPM7. The channels, all with and and and recently into and TRPM C. Rev. PubMed Scopus Google Scholar, C. PubMed Scopus Google Scholar, C. C. Penner R. PubMed Scopus Google Scholar). of these channels are widely in and and of have for the Ca2+ entry pathways of non-excitable cells. members of the sub-family are store-operated and Ca2+ one of the members is activated by in cell and members of the TRPM sub-family are permeable to including Ca2+ PubMed Scopus Google Scholar, Penner R. Physiol. PubMed Scopus Google Scholar). channels are not voltage-gated and are a wide range of activated. that are Ca2+-permeable Ca2+ influxes that with the driving i.e. with membrane the of Ca2+ entry into immune cells and many non-excitable cells. the of TRPM7 PubMed Scopus Google Scholar, Penner R. PubMed Scopus Google it the best for the Ca2+ for Ca2+ entry in many immune cells. of TRPM7 is with transcripts in and PubMed Scopus Google Scholar, Penner R. PubMed Scopus Google Scholar). the it is not known which cell types this channel or role it in or brain have been and roles in the immune cell of the the cells several types of channels, and are in microglia and the respiratory 1999; PubMed Google Scholar, R. Physiol. Physiol. PubMed Google in R. and of the roles of the channels are not may by a membrane potential and Ca2+ entry, as in R. and of and R.S. Rev. PubMed Scopus Google Scholar). The routes of Ca2+ entry in microglia are have that are permeable to Ca2+ and PubMed Scopus Google and a current to be CRAC PubMed Scopus Google of which Ca2+ influxes that with The of voltage-gated Ca2+ channels Physiol. PubMed Google is but a Ca2+ influx. The of Ca2+-permeable channels in microglia has not been In the we have identified transcripts for TRPM7 and characterized a prevalent current in rat brain microglia that has the hallmark features of expressed TRPM7 channels. The same current was expressed in microglia, of from the as as in microglia cultured under a wide range of conditions that favor the resting or activated cell state. There is little known about how members of the TRPM sub-family normally become activated. TRPM7 an kinase it and in the reduce the current PubMed Scopus Google Scholar). it appears that of may be of of TRPM7 channel activation by intracellular Mg2+ Penner R. Physiol. PubMed Scopus Google Scholar, Penner R. PubMed Scopus Google which is a of cation or metal cation Penner R. Physiol. PubMed Scopus Google Scholar, Physiol. PubMed Scopus Google Scholar, R.S. Physiol. PubMed Scopus Google PubMed Google Scholar). this in the whole-cell and patch clamp recordings on rat found that the TRPM7-like current activates spontaneously after but current in The was inhibited by intracellular Mg2+ concentrations. 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PubMed Scopus Google or to as is the CRAC current R.S. Physiol. PubMed Scopus Google Scholar). with Ca2+ to effect on cloned TRPM7 channels PubMed Scopus Google Scholar). However, there was a of current by The current and when Mg2+ was In the of current was by a found previously Penner R. PubMed Scopus Google to inhibit cloned TRPM7 channels. The of Mg2+ with the and into were when Mg2+ was and when Mg2+ was Mg2+ in cells are PubMed Google Scholar, PubMed Scopus Google Scholar). increasing Mg2+ this for the in we current in the not The of this current by intracellular Mg2+ is with cloned TRPM7 and TRPM7-like channels in cells Penner R. Physiol. PubMed Scopus Google Scholar, Physiol. PubMed Scopus Google Scholar, R.S. Physiol. PubMed Scopus Google Scholar, Penner R. Physiol. PubMed Scopus Google Scholar, Penner R. PubMed Scopus Google Scholar, PubMed Google Scholar). the were after were about with and Mg2+ with with is that by Mg2+ more current to as a several on a known of TRPM7 channels, 2-aminoethyldiphenyl a non-selective cation channel and known of ion channels in and 5-nitro-2-(3-phenylpropylamino)benzoic In the was the or for of the channel, and different cells were used for and were of the drugs not be to current in recordings there was by the used for was not but all were a The TRPM7 Penner R. Physiol. PubMed Scopus Google Scholar, R.S. Physiol. PubMed Scopus Google inhibited the current in i.e. by The of the CRAC to TRPM7-like channels is with in one study R.S. Physiol. PubMed Scopus Google and in Physiol. PubMed Scopus Google Scholar). of the TRPM7-like current by not The and which CRAC channels Penner R. Physiol. PubMed Scopus Google Scholar, C. R. C. PubMed Scopus Google reduce cloned or TRPM7 C. Rev. PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, Penner R. Physiol. 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