Research progress on mechanosensitive ion channel protein Piezo1 in infection-related diseases

doi:10.3877/cma.j.issn.1674-1358.2024.05.002

Abstract

Abstract:

Piezo1 is a novel mechanosensitive ion channel protein （MSCP）， which was discovered in 2010 in the Neuro2A neuroblastoma cell line and encoded by the Fam38a gene. Piezo1 is widely expressed in various organs and cells， such as lung， skin， bladder， kidney， endothelial cells and red blood cells. It is activated by mechanical stimulation， regulating intracellular and extracellular Ca²⁺ concentration to modulate downstream intracellular signaling pathways. Recent studies have shown that Piezo1 plays an important role in the occurrence and development of infectious diseases. This article reviews the basic physiological functions and regulatory mechanisms of Piezo1， its functions in immune cells， and its relationship with infection-related diseases， which intended to provide new diagnostic and therapeutic strategies for the clinical prevention and treatment of infection-related diseases.

Key words: Piezo1, Mechanosensitive ion channel protein, Immune cells, Infection-related diseases

Huan Liu, Hao Xing, Zhengqi Chang, Ji Zhang. Research progress on mechanosensitive ion channel protein Piezo1 in infection-related diseases[J]. Chinese Journal of Experimental and Clinical Infectious Diseases(Electronic Edition), 2024, 18(05): 263-269.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://zhsyhlcgrbzz.cma-cmc.com.cn/EN/10.3877/cma.j.issn.1674-1358.2024.05.002

https://zhsyhlcgrbzz.cma-cmc.com.cn/EN/Y2024/V18/I05/263

Figures/Tables 2

References 75

［33］	Friedemann M， Kalbitzer L， Franz S， et al. Instructing human macrophage polarization by stiffness and glycosaminoglycan functionalization in 3D collagen networks［J］. Adv Healthc Mater，2017，6（7）：1600967.
［34］	Geng J， Shi Y， Zhang J， et al. TLR4 signalling via Piezo1 engages and enhances the macrophage mediated host response during bacterial infection［J］. Nat Commun，2021，12（1）：3519.
［35］	Solis AG， Bielecki P， Steach HR， et al. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity［J］.Nature，2019，573（7772）：69-74.
［36］	Atcha H， Jairaman A， Holt JR， et al. Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing［J］. Nat Commun，2021，12（1）：3256.
［37］	Lim TS， Mortellaro A， Lim CT， et al. Mechanical interactions between dendritic cells and T cells correlate with T cell responsiveness［J］. J Immunol，2011，187（1）：258-265.
［38］	Blumenthal D， Chandra V， Avery L， et al. Mouse T cell priming is enhanced by maturation-dependent stiffening of the dendritic cell cortex［J］. Elife，2020，9：e55995.
［39］	Hope JM， Dombroski JA， Pereles RS， et al. Fluid shear stress enhances T cell activation through Piezo1［J］. BMC Biol，2022，20（1）：61.
［40］	Le Borgne M， Raju S， Zinselmeyer BH， et al. Real-time analysis of calcium signals during the early phase of T cell activation using a genetically encoded calcium biosensor［J］. J Immunol，2016，196（4）：1471-1479.
［41］	Liu X， Berry CT， Ruthel G， et al. T cell receptor-induced nuclear factor kappaB （NF-kappaB） signaling and transcriptional activation are regulated by STIM1- and Orai1-mediated calcium entry［J］. J Biol Chem，2016，291（16）：8440-8452.
［42］	Feske S， Giltnane J， Dolmetsch R， et al. Gene regulation mediated by calcium signals in T lymphocytes［J］. Nat Immunol，2001，2（4）：316-324.
［43］	Fehr T， Lucas CL， Kurtz J， et al. A CD8 T cell-intrinsic role for the calcineurin-NFAT pathway for tolerance induction in vivo［J］.Blood，2010，115（6）：1280-1287.
［44］	Vaeth M， Feske S. NFAT control of immune function：New frontiers for an abiding trooper［J］. F1000Res，2018，7：260.
［45］	Liu CSC， Raychaudhuri D， Paul B， et al. Cutting edge：Piezo1 mechanosensors optimize human T cell activation［J］. J Immunol，2018，200（4）：1255-1260.
［46］	Torres A， Cilloniz C， Niederman MS， et al. Pneumonia［J］. Nat Rev Dis Primers，2021，7（1）：25.
［47］	Lin C， Zheng X， Lin S， et al. Mechanotransduction regulates the interplays between alveolar epithelial and vascular endothelial cells in lung［J］. Front Physiol，2022，13：818394.
［48］	Diem K， Fauler M， Fois G， et al. Mechanical stretch activates piezo1 in caveolae of alveolar type Ⅰ cells to trigger ATP release and paracrine stimulation of surfactant secretion from alveolar type Ⅱ cells［J］. FASEB J，2020，34（9）：12785-12804.
［49］	Zhong M， Wu W， Kang H， et al. Alveolar stretch activation of endothelial Piezo1 protects adherens junctions and lung vascular barrier［J］. Am J Respir Cell Mol Biol，2020，62（2）：168-177.
［50］	Chen J， Rodriguez M， Miao J， et al. Mechanosensitive channel Piezo1 is required for pulmonary artery smooth muscle cell proliferation［J］.Am J Physiol Lung Cell Mol Physiol，2022，322（5）：L737-L760.
［51］	Liang GP， Xu J， Cao LL， et al. Piezo1 induced apoptosis of type Ⅱpneumocytes during ARDS［J］. Respir Res，2019，20（1）：118.
［52］	Sato Y， Tansho-Nagakawa S， Ubagai T， et al. Analysis of immune responses in Acinetobacter baumannii-infected Klotho knockout mice：A mouse model of Acinetobacter baumannii infection in aged hosts［J］. Front Immunol，2020，11：601614.
［53］	Mukhopadhyay A， Tsukasaki Y， Chan WC， et al. trans-Endothelial neutrophil migration activates bactericidal function via Piezo1 mechanosensing［J］. Immunity，2024，57（1）：52-67. e10.
［54］	Yang K， Liu S， Yan H， et al. SARS-CoV-2 spike protein receptorbinding domain perturbates intracellular calcium homeostasis and impairs pulmonary vascular endothelial cells［J］. Signal Transduct Target Ther，2023，8（1）：276.
［55］	Zhang M， Wang Q R， Hou X， et al. Blockage of mechanosensitive Piezo1 channel alleviates the severity of experimental malariaassociated acute lung injury［J］. Parasit Vectors，2024，17（1）：46.
［56］	Lin GL， McGinley JP， Drysdale SB， et al. Epidemiology and immune pathogenesis of viral sepsis［J］. Front Immunol，2018，9：2147.
［57］	Font MD， Thyagarajan B， Khanna AK. Sepsis and septic shockbasics of diagnosis， pathophysiology and clinical decision making［J］.Med Clin North Am，2020，104（4）：573-585.
［58］	Angus DC， van der Poll T. Severe sepsis and septic shock［J］. N Engl J Med，2013，369（9）：840-851.
［59］	Aykut B， Chen R， Kim JI， et al. Targeting Piezo1 unleashes innate immunity against cancer and infectious disease［J］. Sci Immunol，2020，5（50）：eabb5168.
［60］	Raia L， Zafrani L. Endothelial activation and microcirculatory disorders in sepsis［J］. Front Med （Lausanne），2022，9：907992.
［61］	Ince C， Sinaasappel M. Microcirculatory oxygenation and shunting in sepsis and shock［J］. Crit Care Med，1999，27（7）：1369-1377.
［62］	Rong S， Zhang L， Wang J， et al. Regulatory role of Piezo1 channel in endothelium-dependent hyperpolarization-mediated vasorelaxation of small resistance vessels and its anti-inflammatory action［J］. Life Sci，2024，336：122326.
［63］	Zhu W， Guo S， Homilius M， et al. PIEZO1 mediates a mechanothrombotic pathway in diabetes［J］. Sci Transl Med，2022，14（626）：eabk1707.
［64］	Assimakopoulos SF， Triantos C， Thomopoulos K， et al. Gut-origin sepsis in the critically ill patient：pathophysiology and treatment［J］.Infection，2018，46（6）：751-760.
［65］	Peterson LW， Artis D. Intestinal epithelial cells：regulators of barrier function and immune homeostasis［J］. Nat Rev Immunol，2014，14（3）：141-153.
［66］	Yoseph BP， Klingensmith NJ， Liang Z， et al. Mechanisms of intestinal barrier dysfunction in sepsis［J］. Shock，2016，46（1）：52-59.
［67］	Yan Z， Niu L， Wang S， et al. Intestinal Piezo1 aggravates intestinal barrier dysfunction during sepsis by mediating Ca（2+） influx［J］. J Transl Med，2024，22（1）：332.
［68］	Ebel ER， Kuypers FA， Lin C， et al. Common host variation drives malaria parasite fitness in healthy human red cells［J］. Elife，2021，10：e69808.
［69］	Nguetse CN， Purington N， Ebel ER， et al. A common polymorphism in the mechanosensitive ion channel PIEZO1 is associated with protection from severe malaria in humans［J］. Proc Natl Acad Sci USA，2020，117（16）：9074-9081.
［70］	Ma S， Cahalan S， LaMonte G， et al. Common PIEZO1 Allele in African populations causes RBC dehydration and attenuates plasmodium infection［J］. Cell，2018，173（2）：443-55. e12.
［71］	Glushakova S， Bezrukov L， Waters H， et al. PIEZO1-dependent erythrocyte dehydration as the mechanism for selection of an allele protecting from severe malaria［Z］. 2022.10.1101/2022.03.31.486604
［72］	Lohia R， Allegrini B， Berry L， et al. Pharmacological activation of PIEZO1 in human red blood cells prevents Plasmodium falciparum invasion［J］. Cell Mol Life Sci，2023，80（5）：124.
［73］	Lin YC， Guo YR， Miyagi A， et al. Force-induced conformational changes in PIEZO1［J］. Nature，2019，573（7773）：230-234.
［74］	Fermo E， Bogdanova A， Petkova-Kirova P， et al. Gardos Channelopathy’：a variant of hereditary Stomatocytosis with complex molecular regulation［J］. Sci Rep，2017，7（1）：1744.
［75］	Yui K， Inoue SI. Host-pathogen interaction in the tissue environment during Plasmodium blood-stage infection［J］. Parasite Immunol，2021，43（2）：e12763.
［1］	Barzegari A， Omidi Y， Ostadrahimi A， et al. The role of Piezo proteins and cellular mechanosensing in tuning the fate of transplanted stem cells［J］. Cell Tissue Res，2020，381（1）：1-12.
［2］	Li J， Hou B， Tumova S， et al. Piezo1 integration of vascular architecture with physiological force［J］. Nature，2014，515（7526）：279-282.
［3］	Velasco-Estevez M， Rolle SO， Mampay M， et al. Piezo1 regulates calcium oscillations and cytokine release from astrocytes［J］.Glia，2020，68（1）：145-160.
［4］	Retailleau K， Duprat F， Arhatte M， et al. Piezo1 in smooth muscle cells is involved in hypertension-dependent arterial remodeling［J］.Cell Rep，2015，13（6）：1161-1171.
［5］	Romac JM， Shahid RA， Swain SM， et al. Piezo1 is a mechanically activated ion channel and mediates pressure induced pancreatitis［J］.Nat Commun，2018，9（1）：1715.
［6］	Cahalan SM， Lukacs V， Ranade SS， et al. Piezo1 links mechanical forces to red blood cell volume［J］. Elife，2015，4：e07370.
［7］	Hatem A， Poussereau G， Gachenot M， et al. Dual action of Dooku1 on PIEZO1 channel in human red blood cells［J］. Front Physiol，2023，14：1222983.
［8］	Li J， Chang Z. Case Report：A spinal infection with bilateral psoas abscesses was treated with NPWT to enhance the local infection by increasing the infiltration of neutrophil cells and draining the pus［J］.Front Cell Infect Microbiol，2023，13：1228376.
［9］	Xing W， Yang Y， Bai Y， et al. A comparison of negative pressure and conventional therapy in spine infections：A single-center retrospective study［J］. J Pers Med，2023，13（2）：162.
［10］	Coste B， Mathur J， Schmidt M， et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels［J］.Science，2010，330（6000）：55-60.
［11］	Xu X， Liu S， Liu H， et al. Piezo channels：awesome mechanosensitive structures in cellular mechanotransduction and their role in bone［J］.Int J Mol Sci，2021，22（12）：6429.
［12］	Zhao Q， Zhou H， Chi S， et al. Structure and mechanogating mechanism of the Piezo1 channel［J］. Nature，2018，554（7693）：487-492.
［13］	Syeda R， Florendo MN， Cox CD， et al. Piezo1 channels are inherently mechanosensitive［J］. Cell Rep，2016，17（7）：1739-1746.
［14］	Jiang F， Yin K， Wu K， et al. The mechanosensitive Piezo1 channel mediates heart mechano-chemo transduction ［J］. Nat Commun，2021，12（1）：869.
［15］	Miyamoto T， Mochizuki T， Nakagomi H， et al. Functional role for Piezo1 in stretch-evoked Ca²⁺ influx and ATP release in urothelial cell cultures［J］. J Biol Chem，2014，289（23）：16565-16575.
［16］	Faucherre A， Kissa K， Nargeot J， et al. Piezo1 plays a role in erythrocyte volume homeostasis［J］. Haematologica，2014，99（1）：70-75.
［17］	Cinar E， Zhou S， DeCourcey J， et al. Piezo1 regulates mechanotransductive release of ATP from human RBCs［J］. Proc Natl Acad Sci USA，2015，112（38）：11783-11788.
［18］	Botello-Smith WM， Jiang W， Zhang H， et al. A mechanism for the activation of the mechanosensitive Piezo1 channel by the small molecule Yoda1［J］. Nat Commun，2019，10（1）：4503.
［19］	Wang Y， Chi S， Guo H， et al. A lever-like transduction pathway for long-distance chemical- and mechano-gating of the mechanosensitive Piezo1 channel［J］. Nat Commun，2018，9（1）：1300.
［20］	Bae C， Sachs F， Gottlieb P A. The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4［J］. Biochemistry，2011，50（29）：6295-6300.
［21］	Beqja D， Haidar S， Nikolaev M， et al. Transgenic Tarantula Toxin：A novel tool to study mechanosensitive ion channels in Drosophila［J］. J Insect Physiol，2020，127：104116.
［22］	Gnanasambandam R， Ghatak C， Yasmann A， et al. GsMTx4：Mechanism of inhibiting mechanosensitive ion channels［J］. Biophys J，2017，112（1）：31-45.
［23］	Suchyna TM. Piezo channels and GsMTx4：Two milestones in our understanding of excitatory mechanosensitive channels and their role in pathology［J］. Prog Biophys Mol Biol，2017，130（Pt B）：244-253.
［24］	Blythe NM， Muraki K， Ludlow MJ， et al. Mechanically activated Piezo1 channels of cardiac fibroblasts stimulate p38 mitogenactivated protein kinase activity and interleukin-6 secretion［J］. J Biol Chem，2019，294（46）：17395-17408.
［25］	De Felice D， Alaimo A. Mechanosensitive piezo channels in cancer：focus on altered calcium signaling in cancer cells and in tumor progression［J］. Cancers （Basel），2020，12（7）：1780.
［26］	Coste B， Xiao B， Santos JS， et al. Piezo proteins are pore-forming subunits of mechanically activated channels［J］. Nature，2012，483（7388）：176-181.
［27］	Suchyna TM， Johnson JH， Hamer K， et al. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels［J］. J Gen Physiol，2000，115（5）：583-598.
［28］	Evans EL， Cuthbertson K， Endesh N， et al. Yoda1 analogue （Dooku1）which antagonizes Yoda1-evoked activation of Piezo1 and aortic relaxation［J］. Br J Pharmacol，2018，175（10）：1744-1759.
［29］	Liu S， Pan X， Cheng W， et al. Tubeimoside Ⅰ antagonizes Yoda1-evoked Piezo1 channel activation［J］. Front Pharmacol，2020，11：768.
［30］	Saika S， Veldhuis N， Krizaj D， et al. Editorial：new insights into mechanotransduction by immune cells in physiological and pathological conditions［J］. Front Immunol，2022，13：930362.
［31］	Yan J， Horng T. Lipid metabolism in regulation of macrophage functions［J］. Trends Cell Biol，2020，30（12）：979-989.
［32］	Gruber EJ， Leifer CA. Molecular regulation of TLR signaling in health and disease：mechano-regulation of macrophages and TLR signaling［J］. Innate Immun，2020，26（1）：15-25.

[1]	Long Qian, Xiaofeng Lu, Xingzhou Wang, Junfeng Du, Xiaofei Shen, Wenxian Guan. Research progress on nervous system regulation of immune response to gastrointestinal tumors [J]. Chinese Journal of Operative Procedures of General Surgery(Electronic Edition), 2024, 18(01): 86-89.
[2]	Jie Mei, Rui Xu, Yun Cai, Yichao Zhu. The effects of fibrosis on tumor-infiltrating immune cells——the formation of "armored & cold tumors" [J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2024, 14(05): 257-263.
[3]	Shouqing Cao, Dong Lai, Qilong Jiao, Zhekun An, Xiubin Li. The role of immune cells in renal ischemia-reperfusion injury and repair [J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2024, 14(01): 45-50.
[4]	Linlin Ma, Lin Xie, Xia Huang, Bingyang Xu, Gang Chen. Comparison the effects of domestic sirolimus and the original product on the cells in vitro and in vivo [J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2020, 10(02): 103-109.
[5]	Youle Su. Analysis of the effect of serum TGF-beta, GFAP and the expression of immune cells on the survival rate of patients with malignant glioma after simultaneous intensity modulated radiotherapy [J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2017, 07(06): 322-326.
[6]	Qiong Wu, Guozhen Zhu. Bioinformatic analysis of genes associated with M2 macrophages in membranous nephropathy [J]. Chinese Journal of Kidney Disease Investigation(Electronic Edition), 2023, 12(03): 156-162.
[7]	Yonghong Yang, Ying Yang, Honglei Qi, Furui Liu, Jinyuan Zhu. Application of single-cell sequencing in acute respiratory distress syndrome [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2024, 10(03): 248-252.
[8]	Zongsheng Wu, Jianfeng Xie, Haibo Qiu. Cold-inducible RNA-binding protein and inflammatory response [J]. Chinese Journal of Critical Care & Intensive Care Medicine(Electronic Edition), 2024, 10(01): 42-47.
[9]	Xiangning Ren, Xiaoming Zheng. Research progress of ischemic stroke and peripheral immune response [J]. Chinese Journal of Brain Diseases and Rehabilitation(Electronic Edition), 2023, 13(03): 175-179.
[10]	Guanchao Sun, Jun Wan, Hui Shi. Research progress on the correlation between IgG-related food intolerance and intestinal immune microenvironment [J]. Chinese Journal of Gastrointestinal Endoscopy(Electronic Edition), 2024, 11(03): 200-203.

Please choose a citation manager

Content to export