Login Register Cart 0
Generic placeholder image

Current Molecular Medicine

Editor-in-Chief

ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Research Article

Expression Suppression and Activity Inhibition of TRPM7 Regulate Cytokine Production and Multiple Organ Dysfunction Syndrome During Endotoxemia: a New Target for Sepsis

Author(s): Sebastian Gatica, Felipe Eltit, Juan F. Santibanez, Diego Varela, Claudio Cabello-Verrugio and Felipe Simon*

Volume 19, Issue 8, 2019

Page: [547 - 559] Pages: 13

DOI: 10.2174/1566524019666190709181726

Abstract

Background: Main pathological features detected during sepsis and endotoxemia include over-secretion of pro-inflammatory cytokines and multiorgan dysfunction syndrome (MODS). Unfortunately, current clinical efforts to treat sepsis are unsatisfactory, and mortality remains high. Interestingly, transient receptor potential (TRP) melastatin 7 (TRPM7) ion channel controlling Ca2+ and Mg2+ permeability is involved in cytokine production and inflammatory response. Furthermore, TRPM7 downregulation has been shown to alleviate local symptoms in some models of sepsis, but its effects at a systemic level remain to be explored.

Objective: To test whether TRPM7 mediates cytokine production and MODS during endotoxemia.

Methods: Endotoxemic and sham-endotoxemic rats were subjected to pharmacological inhibition of TRPM7 using carvacrol, or to expression suppression by adenovirus delivery of shRNA (AdVshTRPM7). Then, cytokine and MODS levels in the blood were measured.

Results: Inhibition of TRPM7 with carvacrol and suppression with AdVshTRPM7 were both efficient in inhibiting the over-secretion of pro-inflammatory cytokines TNF-α, IL-1β, IL-6, and IL-12, in endotoxemic rats, without inducing downregulation in blood levels of antiinflammatory cytokines IL-10 and IL-4. Additionally, the use of carvacrol and AdVshTRPM7 significantly prevented liver and pancreas dysfunction, altered metabolic function, and hypoglycemia, induced by endotoxemia. Furthermore, muscle mass wasting and cardiac muscle damage were also significantly reduced by the use of carvacrol and AdVshTRPM7 in endotoxemic rats.

Conclusion: Our results indicate TRPM7 ion channel as a key protein regulating inflammatory responses and MODS during sepsis. Moreover, TRPM7 appears as a novel molecular target for the management of sepsis.

Keywords: Endotoxemia, TRPM7, cytokine, sepsis, organ dysfunction, MODS.

« Previous Next »
[1]
Vincent J-L, Marshall JC, Namendys-Silva SA, et al. ICON investigators. Assessment of the worldwide burden of critical illness: the intensive care over nations (ICON) audit. Lancet Respir Med 2014; 2(5): 380-6.
[http://dx.doi.org/10.1016/S2213-2600(14)70061-X] [PMID: 24740011]
[2]
Fleischmann C, Scherag A, Adhikari NKJ, et al. International forum of acute care trialists. Assessment of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. Am J Respir Crit Care Med 2016; 193(3): 259-72.
[http://dx.doi.org/10.1164/rccm.201504-0781OC] [PMID: 26414292]
[3]
Trzeciak S, Dellinger RP, Parrillo JE, et al. Microcirculatory alterations in resuscitation and shock investigators. Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: Relationship to hemodynamics, oxygen transport, and survival. Ann Emerg Med 2007; 49(1): 88-98. 98.e1-98.e2
[http://dx.doi.org/10.1016/j.annemergmed.2006.08.021] [PMID: 17095120]
[4]
Dellinger RP, Levy MM, Rhodes A, et al. Surviving sepsis campaign guidelines committee including the pediatric subgroup. Surviving sepsis campaign: International guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med 2013; 39(2): 165-228.
[http://dx.doi.org/10.1007/s00134-012-2769-8] [PMID: 23361625]
[5]
Karima R, Matsumoto S, Higashi H, Matsushima K. The molecular pathogenesis of endotoxic shock and organ failure. Mol Med Today 1999; 5(3): 123-32.
[http://dx.doi.org/10.1016/S1357-4310(98)01430-0] [PMID: 10203736]
[6]
Riedemann NC, Guo R-F, Ward PA. The enigma of sepsis. J Clin Invest 2003; 112(4): 460-7.
[http://dx.doi.org/10.1172/JCI200319523] [PMID: 12925683]
[7]
Pinsky MR. Dysregulation of the immune response in severe sepsis. Am J Med Sci 2004; 328(4): 220-9.
[http://dx.doi.org/10.1097/00000441-200410000-00005] [PMID: 15486537]
[8]
Rivers EP, Ahrens T. Improving outcomes for severe sepsis and septic shock: Tools for early identification of at-risk patients and treatment protocol implementation. Crit Care Clin 2008; 24(3)(Suppl.): S1-S47.
[http://dx.doi.org/10.1016/j.ccc.2008.04.002] [PMID: 18634996]
[9]
Winters BD, Eberlein M, Leung J, et al. Long-term mortality and quality of life in sepsis: a systematic review. Crit Care Clin 2010; 38: 1276-83.
[http://dx.doi.org/10.1097/CCM.0b013e3181d8cc1d]
[10]
Simon F, Fernández R. Early lipopolysaccharide-induced reactive oxygen species production evokes necrotic cell death in human umbilical vein endothelial cells. J Hypertens 2009; 27(6): 1202-16.
[http://dx.doi.org/10.1097/HJH.0b013e328329e31c] [PMID: 19307985]
[11]
Becerra A, Echeverría C, Varela D, et al. Transient receptor potential melastatin 4 inhibition prevents lipopolysaccharide-induced endothelial cell death. Cardiovasc Res 2011; 91(4): 677-84.
[http://dx.doi.org/10.1093/cvr/cvr135] [PMID: 21565835]
[12]
Englert JA, Fink MP. The multiple organ dysfunction syndrome and late-phase mortality in sepsis. Curr Infect Dis Rep 2005; 7(5): 335-41.
[http://dx.doi.org/10.1007/s11908-005-0006-0] [PMID: 16107229]
[13]
Baue AE. Sepsis, systemic inflammatory response syndrome, multiple organ dysfunction syndrome, and multiple organ failure: are trauma surgeons lumpers or splitters? J Trauma 2003; 55(5): 997-8.
[http://dx.doi.org/10.1097/01.TA.0000094631.54198.07] [PMID: 14608184]
[14]
Ziesmann MT, Marshall JC. Multiple Organ Dysfunction: The Defining Syndrome of Sepsis. Surg Infect (Larchmt) 2018; 19(2): 184-90.
[http://dx.doi.org/10.1089/sur.2017.298] [PMID: 29360419]
[15]
Vincent J-L, Taccone F, Schmit X. Classification, incidence, and outcomes of sepsis and multiple organ failure. Contrib Nephrol 2007; 156: 64-74.
[http://dx.doi.org/10.1159/000102071] [PMID: 17464116]
[16]
Jairaman A, Yamashita M, Schleimer RP, Prakriya M. Store-Operated Ca2+ Release-Activated Ca2+ Channels Regulate PAR2-Activated Ca2+ Signaling and Cytokine Production in Airway Epithelial Cells. J Immunol 2015; 195(5): 2122-33.
[http://dx.doi.org/10.4049/jimmunol.1500396] [PMID: 26238490]
[17]
Matsumori A, Nishio R, Nose Y. Calcium channel blockers differentially modulate cytokine production by peripheral blood mononuclear cells. Circ J 2010; 74(3): 567-71.
[http://dx.doi.org/10.1253/circj.CJ-09-0467] [PMID: 20118567]
[18]
Heo DK, Lim HM, Nam JH, Lee MG, Kim JY. Regulation of phagocytosis and cytokine secretion by store-operated calcium entry in primary isolated murine microglia. Cell Signal 2015; 27(1): 177-86.
[http://dx.doi.org/10.1016/j.cellsig.2014.11.003] [PMID: 25451082]
[19]
Savignac M, Mellström B, Naranjo JR. Calcium-dependent transcription of cytokine genes in T lymphocytes. Pflugers Arch 2007; 454(4): 523-33.
[http://dx.doi.org/10.1007/s00424-007-0238-y] [PMID: 17334777]
[20]
Dietrich A, Gudermann T. Another TRP to endothelial dysfunction: TRPM2 and endothelial permeability. Circ Res 2008; 102(3): 275-7.
[http://dx.doi.org/10.1161/CIRCRESAHA.107.170548] [PMID: 18276923]
[21]
Nishida M, Hara Y, Yoshida T, Inoue R, Mori Y. TRP channels: molecular diversity and physiological function. Microcirculation 2006; 13(7): 535-50.
[http://dx.doi.org/10.1080/10739680600885111] [PMID: 16990213]
[22]
Scheraga RG, Southern BD, Grove LM, Olman MA. The Role of Transient Receptor Potential Vanilloid 4 in Pulmonary Inflammatory Diseases. Front Immunol 2017; 8: 503.
[http://dx.doi.org/10.3389/fimmu.2017.00503] [PMID: 28523001]
[23]
Dalsgaard T, Sonkusare SK, Teuscher C, Poynter ME, Nelson MT. Pharmacological inhibitors of TRPV4 channels reduce cytokine production, restore endothelial function and increase survival in septic mice. Sci Rep 2016; 6: 33841.
[http://dx.doi.org/10.1038/srep33841] [PMID: 27653046]
[24]
Guptill V, Cui X, Khaibullina A, et al. Disruption of the transient receptor potential vanilloid 1 can affect survival, bacterial clearance, and cytokine gene expression during murine sepsis. Anesthesiology 2011; 114(5): 1190-9.
[http://dx.doi.org/10.1097/ALN.0b013e318212515b] [PMID: 21383614]
[25]
Zhang F, Yang H, Wang Z, et al. Transient receptor potential vanilloid 1 activation induces inflammatory cytokine release in corneal epithelium through MAPK signaling. J Cell Physiol 2007; 213(3): 730-9.
[http://dx.doi.org/10.1002/jcp.21141] [PMID: 17508360]
[26]
Gouin O, L’Herondelle K, Lebonvallet N, et al. TRPV1 and TRPA1 in cutaneous neurogenic and chronic inflammation: pro-inflammatory response induced by their activation and their sensitization. Protein Cell 2017; 8(9): 644-61.
[http://dx.doi.org/10.1007/s13238-017-0395-5] [PMID: 28364279]
[27]
Tsutsui M, Hirase R, Miyamura S, et al. TRPM2 Exacerbates Central Nervous System Inflammation in Experimental Autoimmune Encephalomyelitis by Increasing Production of CXCL2 Chemokines. J Neurosci 2018; 38(39): 8484-95.
[http://dx.doi.org/10.1523/JNEUROSCI.2203-17.2018] [PMID: 30201769]
[28]
Tang R, Li Z-P, Li M-X, et al. Pro-inflammatory role of transient receptor potential canonical channel 6 in the pathogenesis of chronic rhinosinusitis with nasal polyps. Int Forum Allergy Rhinol 2018; 8(11)(Suppl. 1): 1334-41.
[http://dx.doi.org/10.1002/alr.22208] [PMID: 30216703]
[29]
Khalil M, Babes A, Lakra R, et al. Transient receptor potential melastatin 8 ion channel in macrophages modulates colitis through a balance-shift in TNF-alpha and interleukin-10 production. Mucosal Immunol 2016; 9(6): 1500-13.
[http://dx.doi.org/10.1038/mi.2016.16] [PMID: 26982596]
[30]
Yamashiro K, Sasano T, Tojo K, et al. Role of transient receptor potential vanilloid 2 in LPS-induced cytokine production in macrophages. Biochem Biophys Res Commun 2010; 398(2): 284-9.
[http://dx.doi.org/10.1016/j.bbrc.2010.06.082] [PMID: 20599720]
[31]
Wehrhahn J, Kraft R, Harteneck C, Hauschildt S. Transient receptor potential melastatin 2 is required for lipopolysaccharide-induced cytokine production in human monocytes. J Immunol 2010; 184(5): 2386-93.
[http://dx.doi.org/10.4049/jimmunol.0902474] [PMID: 20107186]
[32]
Schlingmann KP, Waldegger S, Konrad M, Chubanov V, Gudermann T. TRPM6 and TRPM7-Gatekeepers of human magnesium metabolism. Biochim Biophys Acta 2007; 1772(8): 813-21.
[http://dx.doi.org/10.1016/j.bbadis.2007.03.009] [PMID: 17481860]
[33]
Huang L, Ng N-M, Chen M, et al. Inhibition of TRPM7 channels reduces degranulation and release of cytokines in rat bone marrow-derived mast cells. Int J Mol Sci 2014; 15(7): 11817-31.
[http://dx.doi.org/10.3390/ijms150711817] [PMID: 24995695]
[34]
Schappe MS, Szteyn K, Stremska ME, et al. Chanzyme TRPM7 Mediates the Ca2+ Influx Essential for Lipopolysaccharide-Induced Toll-Like Receptor 4 Endocytosis and Macrophage Activation. Immunity 2018; 48(1): 59-74.e5.
[http://dx.doi.org/10.1016/j.immuni.2017.11.026] [PMID: 29343440]
[35]
Echeverría C, Montorfano I, Hermosilla T, et al. Endotoxin induces fibrosis in vascular endothelial cells through a mechanism dependent on transient receptor protein melastatin 7 activity. PLoS One 2014; 9(4)e94146
[http://dx.doi.org/10.1371/journal.pone.0094146] [PMID: 24710004]
[36]
Yang C-W, Liu H, Li X-D, Sui SG, Liu YF. Salvianolic acid B protects against acute lung injury by decreasing TRPM6 and TRPM7 expressions in a rat model of sepsis. J Cell Biochem 2018; 119(1): 701-11.
[http://dx.doi.org/10.1002/jcb.26233] [PMID: 28636082]
[37]
Moreno C, Hermosilla T, Morales D, et al. Cavβ2 transcription start site variants modulate calcium handling in newborn rat cardiomyocytes. Pflugers Arch 2015; 467(12): 2473-84.
[http://dx.doi.org/10.1007/s00424-015-1723-3] [PMID: 26265381]
[38]
Parnas M, Peters M, Dadon D, et al. Carvacrol is a novel inhibitor of Drosophila TRPL and mammalian TRPM7 channels. Cell Calcium 2009; 45(3): 300-9.
[http://dx.doi.org/10.1016/j.ceca.2008.11.009] [PMID: 19135721]
[39]
Chen W, Xu B, Xiao A, et al. TRPM7 inhibitor carvacrol protects brain from neonatal hypoxic-ischemic injury. Mol Brain 2015; 8(1): 11.
[http://dx.doi.org/10.1186/s13041-015-0102-5] [PMID: 25761704]
[40]
Chen W-L, Barszczyk A, Turlova E, et al. Inhibition of TRPM7 by carvacrol suppresses glioblastoma cell proliferation, migration and invasion. Oncotarget 2015; 6(18): 16321-40.
[http://dx.doi.org/10.18632/oncotarget.3872] [PMID: 25965832]
[41]
Sun H-S, Jackson MF, Martin LJ, et al. Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neurosci 2009; 12(10): 1300-7.
[http://dx.doi.org/10.1038/nn.2395] [PMID: 19734892]
[42]
Maitra SR, Wojnar MM, Lang CH. Alterations in tissue glucose uptake during the hyperglycemic and hypoglycemic phases of sepsis. Shock 2000; 13(5): 379-85.
[http://dx.doi.org/10.1097/00024382-200005000-00006] [PMID: 10807013]
[43]
Igaki N, Matsuda T, Hirota Y, Kawaguchi T, Tamada F, Goto T. Streptococcal toxic shock syndrome presenting with spontaneous hypoglycemia in a chronic hemodialysis patient: pathophysiological mechanisms. Intern Med 2003; 42(5): 421-3.
[http://dx.doi.org/10.2169/internalmedicine.42.421] [PMID: 12793713]
[44]
Tsai S-H, Lin Y-Y, Hsu C-W, Cheng CS, Chu DM. Hypoglycemia revisited in the acute care setting. Yonsei Med J 2011; 52(6): 898-908.
[http://dx.doi.org/10.3349/ymj.2011.52.6.898] [PMID: 22028152]
[45]
Tracey KJ, Fong Y, Hesse DG, et al. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature 1987; 330(6149): 662-4.
[http://dx.doi.org/10.1038/330662a0] [PMID: 3317066]
[46]
Douzinas EE, Tsidemiadou PD, Pitaridis MT, et al. The regional production of cytokines and lactate in sepsis-related multiple organ failure. Am J Respir Crit Care Med 1997; 155(1): 53-9.
[http://dx.doi.org/10.1164/ajrccm.155.1.9001289] [PMID: 9001289]
[47]
Pinsky MR. Clinical studies on cytokines in sepsis: role of serum cytokines in the development of multiple-systems organ failure. Nephrol Dial Transplant 1994; 9(Suppl. 4): 94-8.
[PMID: 7800275]
[48]
Yang FL, Li CH, Hsu BG, et al. The reduction of tumor necrosis factor-alpha release and tissue damage by pentobarbital in the experimental endotoxemia model. Shock 2007; 28(3): 309-16.
[PMID: 17545946]
[49]
Levy MM, Fink MP, Marshall JC, et al. SCCM/ESICM/ACCP/ATS/SIS 2001 SCCM/ESICM/ACCP/ATS/SIS. International Sepsis Definitions Conference. Crit Care Med 2003; 31(4): 1250-6.
[http://dx.doi.org/10.1097/01.CCM.0000050454.01978.3B] [PMID: 12682500]
[50]
Levy MM, Fink MP, Marshall JC, et al. International Sepsis Definitions Conference. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Intensive Care Med 2003; 29(4): 530-8.
[http://dx.doi.org/10.1007/s00134-003-1662-x] [PMID: 12664219]
[51]
Wykes RCE, Lee M, Duffy SM, Yang W, Seward EP, Bradding P. Functional transient receptor potential melastatin 7 channels are critical for human mast cell survival. J Immunol 2007; 179(6): 4045-52.
[http://dx.doi.org/10.4049/jimmunol.179.6.4045] [PMID: 17785843]
[52]
Sahni J, Tamura R, Sweet IR, Scharenberg AM. TRPM7 regulates quiescent/proliferative metabolic transitions in lymphocytes. Cell Cycle 2010; 9(17): 3565-74.
[http://dx.doi.org/10.4161/cc.9.17.12798] [PMID: 20724843]
[53]
Du J, Xie J, Zhang Z, et al. TRPM7-mediated Ca2+ signals confer fibrogenesis in human atrial fibrillation. Circ Res 2010; 106(5): 992-1003.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.206771] [PMID: 20075334]
[54]
Hermosura MC, Garruto RM. TRPM7 and TRPM2-Candidate susceptibility genes for Western Pacific ALS and PD? Biochim Biophys Acta 2007; 1772(8): 822-35.
[http://dx.doi.org/10.1016/j.bbadis.2007.02.008] [PMID: 17395433]
[55]
McNeill MS, Paulsen J, Bonde G, Burnight E, Hsu MY, Cornell RA. Cell death of melanophores in zebrafish trpm7 mutant embryos depends on melanin synthesis. J Invest Dermatol 2007; 127(8): 2020-30.
[http://dx.doi.org/10.1038/sj.jid.5700710] [PMID: 17290233]
[56]
Kim BJ, Nah S-Y, Jeon J-H, So I, Kim SJ. Transient receptor potential melastatin 7 channels are involved in ginsenoside Rg3-induced apoptosis in gastric cancer cells. Basic Clin Pharmacol Toxicol 2011; 109(4): 233-9.
[http://dx.doi.org/10.1111/j.1742-7843.2011.00706.x] [PMID: 21443732]
[57]
Tauseef M, Knezevic N, Chava KR, et al. TLR4 activation of TRPC6-dependent calcium signaling mediates endotoxin-induced lung vascular permeability and inflammation. J Exp Med 2012; 209(11): 1953-68.
[http://dx.doi.org/10.1084/jem.20111355] [PMID: 23045603]
[58]
Park HS, Chun JN, Jung HY, Choi C, Bae YS. Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells. Cardiovasc Res 2006; 72(3): 447-55.
[http://dx.doi.org/10.1016/j.cardiores.2006.09.012] [PMID: 17064675]
[59]
Nadler MJ, Hermosura MC, Inabe K, et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 2001; 411(6837): 590-5.
[http://dx.doi.org/10.1038/35079092] [PMID: 11385574]
[60]
Aarts M, Iihara K, Wei WL, et al. A key role for TRPM7 channels in anoxic neuronal death. Cell 2003; 115(7): 863-77.
[http://dx.doi.org/10.1016/S0092-8674(03)01017-1] [PMID: 14697204]
[61]
Wuensch T, Thilo F, Krueger K, Scholze A, Ristow M, Tepel M. High glucose-induced oxidative stress increases transient receptor potential channel expression in human monocytes. Diabetes 2010; 59(4): 844-9.
[http://dx.doi.org/10.2337/db09-1100] [PMID: 20068131]
[62]
Nuñez-Villena F, Becerra A, Echeverría C, et al. Increased expression of the transient receptor potential melastatin 7 channel is critically involved in lipopolysaccharide-induced reactive oxygen species-mediated neuronal death. Antioxid Redox Signal 2011; 15(9): 2425-38.
[http://dx.doi.org/10.1089/ars.2010.3825] [PMID: 21539414]
[63]
Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 1997; 386(6627): 855-8.
[http://dx.doi.org/10.1038/386855a0] [PMID: 9126747]
[64]
Brough D, Le Feuvre RA, Wheeler RD, et al. Ca2+ stores and Ca2+ entry differentially contribute to the release of IL-1 beta and IL-1 alpha from murine macrophages. J Immunol 2003; 170(6): 3029-36.
[http://dx.doi.org/10.4049/jimmunol.170.6.3029] [PMID: 12626557]
[65]
Novotny AR, Reim D, Assfalg V, et al. Mixed antagonist response and sepsis severity-dependent dysbalance of pro- and anti-inflammatory responses at the onset of postoperative sepsis. Immunobiology 2012; 217(6): 616-21.
[http://dx.doi.org/10.1016/j.imbio.2011.10.019] [PMID: 22204813]
[66]
Rittirsch D, Flierl MA, Ward PA. Harmful molecular mechanisms in sepsis. Nat Rev Immunol 2008; 8(10): 776-87.
[http://dx.doi.org/10.1038/nri2402] [PMID: 18802444]
[67]
Luzina IG, Keegan AD, Heller NM, Rook GA, Shea-Donohue T, Atamas SP. Regulation of inflammation by interleukin-4: a review of “alternatives”. J Leukoc Biol 2012; 92(4): 753-64.
[http://dx.doi.org/10.1189/jlb.0412214] [PMID: 22782966]
[68]
Gessner A, Mohrs K, Mohrs M. Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J Immunol 2005; 174(2): 1063-72.
[http://dx.doi.org/10.4049/jimmunol.174.2.1063] [PMID: 15634931]
[69]
Reinhart R, Kaufmann T. IL-4 enhances survival of in vitro-differentiated mouse basophils through transcription-independent signaling downstream of PI3K. Cell Death Dis 2018; 9(7): 713.
[http://dx.doi.org/10.1038/s41419-018-0754-z] [PMID: 29915306]
[70]
Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection. J Immunol 2008; 180(9): 5771-7.
[http://dx.doi.org/10.4049/jimmunol.180.9.5771] [PMID: 18424693]
[71]
Rojas JM, Avia M, Martín V, Sevilla N. IL-10: A Multifunctional Cytokine in Viral Infections. J Immunol Res 2017; 2017(4): 6104054-14.
[http://dx.doi.org/10.1155/2017/6104054] [PMID: 28316998]
[72]
Vaeth M, Feske S. Ion channelopathies of the immune system. Curr Opin Immunol 2018; 52: 39-50.
[http://dx.doi.org/10.1016/j.coi.2018.03.021] [PMID: 29635109]
[73]
Freichel M, Almering J, Tsvilovskyy V. The Role of TRP Proteins in Mast Cells. Front Immunol 2012; 3: 150.
[http://dx.doi.org/10.3389/fimmu.2012.00150] [PMID: 22701456]
[74]
Iyer SS, Cheng G. Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Crit Rev Immunol 2012; 32(1): 23-63.
[http://dx.doi.org/10.1615/CritRevImmunol.v32.i1.30] [PMID: 22428854]
[75]
Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003; 4(7): 517-29.
[http://dx.doi.org/10.1038/nrm1155] [PMID: 12838335]
[76]
Simon F, Stutzin A. Protein kinase C-mediated phosphorylation of p47 phox modulates platelet-derived growth factor-induced H2O2 generation and cell proliferation in human umbilical vein endothelial cells. Endothelium 2008; 15(4): 175-88.
[http://dx.doi.org/10.1080/10623320802174480] [PMID: 18663621]
[77]
Targos B, Barańska J, Pomorski P. Store-operated calcium entry in physiology and pathology of mammalian cells. Acta Biochim Pol 2005; 52(2): 397-409.
[PMID: 15933763]
[78]
Gotru SK, Chen W, Kraft P, et al. TRPM7 Kinase Controls Calcium Responses in Arterial Thrombosis and Stroke in Mice. Arterioscler Thromb Vasc Biol 2018; 38(2): 344-52.
[http://dx.doi.org/10.1161/ATVBAHA.117.310391] [PMID: 29146750]
[79]
Romagnani A, Vettore V, Rezzonico-Jost T, et al. TRPM7 kinase activity is essential for T cell colonization and alloreactivity in the gut. Nat Commun 2017; 8(1): 1917.
[http://dx.doi.org/10.1038/s41467-017-01960-z] [PMID: 29203869]
[80]
Clapham DE, Runnels LW, Strübing C. The TRP ion channel family. Nat Rev Neurosci 2001; 2(6): 387-96.
[http://dx.doi.org/10.1038/35077544] [PMID: 11389472]
[81]
Runnels LW, Yue L, Clapham DE. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 2001; 291(5506): 1043-7.
[http://dx.doi.org/10.1126/science.1058519] [PMID: 11161216]

Rights & Permissions Print Cite
Article Metrics
39
3
1
1
© 2024 Bentham Science Publishers | Privacy Policy