Volume 5 Issue 1
Jun.  2021
Turn off MathJax
Article Contents
Xiaowei Sun, Wenyue Zheng, Rui Hua, Yujie Liu, Li Wang, Yun-Gi Kim, Xinqi Liu, Hitomi Mimuro, Zhongyang Shen, Lian Li, Sei Yoshida. Macropinocytosis and SARS-CoV-2 cell entry[J]. Blood&Genomics, 2021, 5(1): 1-12. doi: 10.46701/BG.2021012021110
Citation: Xiaowei Sun, Wenyue Zheng, Rui Hua, Yujie Liu, Li Wang, Yun-Gi Kim, Xinqi Liu, Hitomi Mimuro, Zhongyang Shen, Lian Li, Sei Yoshida. Macropinocytosis and SARS-CoV-2 cell entry[J]. Blood&Genomics, 2021, 5(1): 1-12. doi: 10.46701/BG.2021012021110

Macropinocytosis and SARS-CoV-2 cell entry

doi: 10.46701/BG.2021012021110
More Information
  • Corresponding author: Zhongyang Shen, Organ Transplant Department, Tianjin First Central Hospital, Tianjin 300192, China. E-mail: zhongyangshen@vip.sina.com; Lian Li, State Key Laboratory of Medicinal Chemical Biology, College of Life Sciences, Frontiers Science Center for Cell Responses, Nankai University, No. 94 Weijin Road, Tianjin 300071, China. E-mail: lilian523@nankai.edu.cn; Sei Yoshida, State Key Laboratory of Medicinal Chemical Biology, College of Life Sciences, Frontiers Science Center for Cell Responses, Nankai University, No. 94, Weijin Road, Tianjin 300071, China. E-mail: seiyoshi@nankai.edu.cn
  • Received Date: 2021-04-05
  • Accepted Date: 2021-05-08
  • Rev Recd Date: 2021-04-25
  • Publish Date: 2021-06-01
  • Macropinocytosis is a type of large-scale endocytosis that is triggered by the interaction of receptor proteins and ligands, such as growth factors, cytokines, chemokines, and lipopolysaccharide (LPS). Macropinocytosis ingests the extracellular fluid solutes and conveys them into the lysosome in the context of cell growth and differentiation. Aside from its physiological functions, macropinocytosis has been observed in viral infections. While the infectious mechanism of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is still unknown, recent studies suggest the involvement of macropinocytosis in its cell entry. In this review, we discuss the roles of endocytosis in SARS-CoV/SARS-CoV-2 cell entries and propose a hypothetical role of macropinocytosis in SARS-CoV-2 cell entry.

     

  • These authors contributed equally to this work.
  • loading
  • [1]
    Swanson JA. Phosphoinositides and engulfment[J]. Cell Microbiol, 2014, 16(10): 1473−1483. doi: 10.1111/cmi.12334
    [2]
    Phuyal S, Farhan H. Multifaceted Rho GTPase signaling at the endomembranes[J]. Front Cell Dev Biol, 2019, 7: 127. doi: 10.3389/fcell.2019.00127
    [3]
    Schaks M, Giannone G, Rottner K. Actin dynamics in cell migration[J]. Essays Biochem, 2019, 63(5): 483−495. doi: 10.1042/EBC20190015
    [4]
    Mettlen M, Chen PH, Srinivasan S, et al. Regulation of clathrin-mediated endocytosis[J]. Annu Rev Biochem, 2018, 87: 871−896. doi: 10.1146/annurev-biochem-062917-012644
    [5]
    Parton RG, McMahon KA, Wu YP. Caveolae: formation, dynamics, and function[J]. Curr Opin Cell Biol, 2020, 65: 8−16. doi: 10.1016/j.ceb.2020.02.001
    [6]
    Swanson JA. Shaping cups into phagosomes and macropinosomes[J]. Nat Rev Mol Cell Biol, 2008, 9(8): 639−649. doi: 10.1038/nrm2447
    [7]
    Cossart P, Helenius A. Endocytosis of viruses and bacteria[J]. Cold Spring Harb Perspect Biol, 2014, 6(8): a016972. doi: 10.1101/cshperspect.a016972
    [8]
    Yoshida S, Pacitto R, Inoki K, et al. Macropinocytosis, mTORC1 and cellular growth control[J]. Cell Mol Life Sci, 2018, 75(7): 1227−1239. doi: 10.1007/s00018-017-2710-y
    [9]
    Buckley CM, King JS. Drinking problems: mechanisms of macropinosome formation and maturation[J]. FEBS J, 2017, 284(22): 3778−3790. doi: 10.1111/febs.14115
    [10]
    Stow JL, Hung Y, Wall AA. Macropinocytosis: insights from immunology and cancer[J]. Curr Opin Cell Biol, 2020, 65: 131−140. doi: 10.1016/j.ceb.2020.06.005
    [11]
    Mercer J, Helenius A. Gulping rather than sipping: macropinocytosis as a way of virus entry[J]. Curr Opin Microbiol, 2012, 15(4): 490−499. doi: 10.1016/j.mib.2012.05.016
    [12]
    Yoshida S, Sasakawa C. Exploiting host microtubule dynamics: a new aspect of bacterial invasion[J]. Trends Microbiol, 2003, 11(3): 139−143. doi: 10.1016/S0966-842X(03)00023-4
    [13]
    Hume PJ, Singh V, Davidson AC, et al. Swiss army pathogen: the Salmonella entry toolkit[J]. Front Cell Infect Microbiol, 2017, 7: 348. doi: 10.3389/fcimb.2017.00348
    [14]
    Mercer J, Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells[J]. Science, 2008, 320(5875): 531−535. doi: 10.1126/science.1155164
    [15]
    Quinn K, Brindley MA, Weller ML, et al. Rho GTPases modulate entry of Ebola virus and vesicular stomatitis virus pseudotyped vectors[J]. J Virol, 2009, 83(19): 10176−10186. doi: 10.1128/JVI.00422-09
    [16]
    Glebov OO. Understanding SARS-CoV-2 endocytosis for COVID-19 drug repurposing[J]. FEBS J, 2020, 287(17): 3664−3671. doi: 10.1111/febs.15369
    [17]
    Dubielecka PM, Cui P, Xiong XL, et al. Differential regulation of macropinocytosis by Abi1/Hssh3bp1 isoforms[J]. PLoS One, 2010, 5(5): e10430. doi: 10.1371/journal.pone.0010430
    [18]
    Balaji K, Mooser C, Janson CM, et al. RIN1 orchestrates the activation of RAB5 GTPases and ABL tyrosine kinases to determine the fate of EGFR[J]. J Cell Sci, 2012, 125(Pt 23): 5887−5896. doi: 10.1242/jcs.113688
    [19]
    Krishna S, Palm W, Lee Y, et al. PIKfyve regulates vacuole maturation and nutrient recovery following engulfment[J]. Dev Cell, 2016, 38(5): 536−547. doi: 10.1016/j.devcel.2016.08.001
    [20]
    Ou XY, Liu Y, Lei XB, et al. Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV[J]. Nat Commun, 2020, 11(1): 1620. doi: 10.1038/s41467-020-15562-9
    [21]
    Mulgaonkar N, Wang HQ, Mallawarachchi S, et al. Bcr-Abl tyrosine kinase inhibitor imatinib as a potential drug for COVID-19[EB/OL]. bioRxiv, 2020.
    [22]
    Mugisha CS, Vuong HR, Puray-Chavez M, et al. A facile Q-RT-PCR assay for monitoring SARS-CoV-2 growth in cell culture[EB/OL]. bioRxiv, 2020.
    [23]
    Chan JF, Kok KH, Zhu Z, et al. Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan[J]. Emerg Microbes Infect, 2020, 9(1): 221−236. doi: 10.1080/22221751.2020.1719902
    [24]
    Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin[J]. Nature, 2020, 579(7798): 270−273. doi: 10.1038/s41586-020-2012-7
    [25]
    Yang ND, Shen HM. Targeting the endocytic pathway and autophagy process as a novel therapeutic strategy in COVID-19[J]. Int J Biol Sci, 2020, 16(10): 1724−1731. doi: 10.7150/ijbs.45498
    [26]
    Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis[J]. Annu Rev Biochem, 2010, 79: 803−833. doi: 10.1146/annurev-biochem-060208-104626
    [27]
    Dutta D, Donaldson JG. Search for inhibitors of endocytosis: intended specificity and unintended consequences[J]. Cell Logist, 2012, 2(4): 203−208. doi: 10.4161/cl.23967
    [28]
    Baschieri F, Porshneva K, Montagnac G. Frustrated clathrin-mediated endocytosis-causes and possible functions[J]. J Cell Sci, 2020, 133(11): jcs240861. doi: 10.1242/jcs.240861
    [29]
    Wang LH, Rothberg KG, Anderson RG. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation[J]. J Cell Biol, 1993, 123(5): 1107−1117. doi: 10.1083/jcb.123.5.1107
    [30]
    Macia E, Ehrlich M, Massol R, et al. Dynasore, a cell-permeable inhibitor of dynamin[J]. Dev Cell, 2006, 10(6): 839−850. doi: 10.1016/j.devcel.2006.04.002
    [31]
    Dutta D, Williamson CD, Cole NB, et al. Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis[J]. PLoS One, 2012, 7(9): e45799. doi: 10.1371/journal.pone.0045799
    [32]
    Sieczkarski SB, Whittaker GR. Dissecting virus entry via endocytosis[J]. J Gen Virol, 2002, 83(Pt 7): 1535−1545. doi: 10.1099/0022-1317-83-7-1535
    [33]
    Sandvig K, Kavaliauskiene S, Skotland T. Clathrin-independent endocytosis: an increasing degree of complexity[J]. Histochem Cell Biol, 2018, 150(2): 107−118. doi: 10.1007/s00418-018-1678-5
    [34]
    Rodal SK, Skretting G, Garred Ø, et al. Extraction of cholesterol with methyl-β-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles[J]. Mol Biol Cell, 1999, 10(4): 961−974. doi: 10.1091/mbc.10.4.961
    [35]
    Schnitzer JE, Oh P, Pinney E, et al. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules[J]. J Cell Biol, 1994, 127(5): 1217−1232. doi: 10.1083/jcb.127.5.1217
    [36]
    Anderson HA, Chen Y, Norkin LC. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae[J]. Mol Biol Cell, 1996, 7(11): 1825−1834. doi: 10.1091/mbc.7.11.1825
    [37]
    Egami Y, Taguchi T, Maekawa M, et al. Small GTPases and phosphoinositides in the regulatory mechanisms of macropinosome formation and maturation[J]. Front Physiol, 2014, 5: 374. doi: 10.3389/fphys.2014.00374
    [38]
    Swanson JA, King JS. The breadth of macropinocytosis research[J]. Philos Trans R Soc Lond B Biol Sci, 2019, 374(1765): 20180146. doi: 10.1098/rstb.2018.0146
    [39]
    Yoshida S, Hoppe AD, Araki N, et al. Sequential signaling in plasma-membrane domains during macropinosome formation in macrophages[J]. J Cell Sci, 2009, 122(18): 3250−3261. doi: 10.1242/jcs.053207
    [40]
    Yoshida S, Gaeta I, Pacitto R, et al. Differential signaling during macropinocytosis in response to M-CSF and PMA in macrophages[J]. Front Physiol, 2015, 6: 8. doi: 10.3389/fphys.2015.00008
    [41]
    Lanier MH, Kim T, Cooper JA. CARMIL2 is a novel molecular connection between vimentin and actin essential for cell migration and invadopodia formation[J]. Mol Biol Cell, 2015, 26(25): 4577−4588. doi: 10.1091/mbc.E15-08-0552
    [42]
    Williamson CD, Donaldson JG. Arf6, JIP3, and dynein shape and mediate macropinocytosis[J]. Mol Biol Cell, 2019, 30(12): 1477−1489. doi: 10.1091/mbc.E19-01-0022
    [43]
    Feliciano WD, Yoshida S, Straight SW, et al. Coordination of the Rab5 cycle on macropinosomes[J]. Traffic, 2011, 12(12): 1911−1922. doi: 10.1111/j.1600-0854.2011.01280.x
    [44]
    Koivusalo M, Welch C, Hayashi H, et al. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling[J]. J Cell Biol, 2010, 188(4): 547−563. doi: 10.1083/jcb.200908086
    [45]
    Maekawa M, Terasaka S, Mochizuki Y, et al. Sequential breakdown of 3-phosphorylated phosphoinositides is essential for the completion of macropinocytosis[J]. Proc Natl Acad Sci USA, 2014, 111(11): E978−E987. doi: 10.1073/pnas.1311029111
    [46]
    Li HA, Marshall AJ. Phosphatidylinositol (3,4) bisphosphate-specific phosphatases and effector proteins: a distinct branch of PI3K signaling[J]. Cell Signal, 2015, 27(9): 1789−1798. doi: 10.1016/j.cellsig.2015.05.013
    [47]
    Porat-Shliom N, Kloog Y, Donaldson JG. A unique platform for H-Ras signaling involving clathrin-independent endocytosis[J]. Mol Biol Cell, 2008, 19(3): 765−775. doi: 10.1091/mbc.e07-08-0841
    [48]
    Belouzard S, Millet JK, Licitra BN, et al. Mechanisms of coronavirus cell entry mediated by the viral spike protein[J]. Viruses, 2012, 4(6): 1011−1033. doi: 10.3390/v4061011
    [49]
    Fung TS, Liu DX. Human coronavirus: host-pathogen interaction[J]. Annu Rev Microbiol, 2019, 73: 529−557. doi: 10.1146/annurev-micro-020518-115759
    [50]
    Xiao XD, Chakraborti S, Dimitrov AS, et al. The SARS-CoV S glycoprotein: expression and functional characterization[J]. Biochem Biophys Res Commun, 2003, 312(4): 1159−1164. doi: 10.1016/j.bbrc.2003.11.054
    [51]
    Millet JK, Whittaker GR. Host cell proteases: critical determinants of coronavirus tropism and pathogenesis[J]. Virus Res, 2015, 202: 120−134. doi: 10.1016/j.virusres.2014.11.021
    [52]
    Bosch BJ, Van Der Zee R, De Haan CAM, et al. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex[J]. J Virol, 2003, 77(16): 8801−8811. doi: 10.1128/JVI.77.16.8801-8811.2003
    [53]
    Wong SK, Li WH, Moore MJ, et al. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2[J]. J Biol Chem, 2004, 279(5): 3197−3201. doi: 10.1074/jbc.C300520200
    [54]
    Babcock GJ, Esshaki DJ, Thomas Jr WD, et al. Amino acids 270 to 510 of the severe acute respiratory syndrome coronavirus spike protein are required for interaction with receptor[J]. J Virol, 2004, 78(9): 4552−4560. doi: 10.1128/JVI.78.9.4552-4560.2004
    [55]
    Li F, Li WH, Farzan M, et al. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor[J]. Science, 2005, 309(5742): 1864−1868. doi: 10.1126/science.1116480
    [56]
    Belouzard S, Chu VC, Whittaker GR. Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites[J]. Proc Natl Acad Sci USA, 2009, 106(14): 5871−5876. doi: 10.1073/pnas.0809524106
    [57]
    Li F, Berardi M, Li WH, et al. Conformational states of the severe acute respiratory syndrome coronavirus spike protein ectodomain[J]. J Virol, 2006, 80(14): 6794−6800. doi: 10.1128/JVI.02744-05
    [58]
    Bosch BJ, Bartelink W, Rottier PJM. Cathepsin L functionally cleaves the severe acute respiratory syndrome coronavirus class I fusion protein upstream of rather than adjacent to the fusion peptide[J]. J Virol, 2008, 82(17): 8887−8890. doi: 10.1128/JVI.00415-08
    [59]
    Matsuyama S, Nagata N, Shirato K, et al. Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2[J]. J Virol, 2010, 84(24): 12658−12664. doi: 10.1128/JVI.01542-10
    [60]
    Shulla A, Heald-Sargent T, Subramanya G, et al. A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry[J]. J Virol, 2011, 85(2): 873−882. doi: 10.1128/JVI.02062-10
    [61]
    Iwata-Yoshikawa N, Okamura T, Shimizu Y, et al. TMPRSS2 contributes to virus spread and immunopathology in the airways of murine models after coronavirus infection[J]. J Virol, 2019, 93(6): e01815−18. doi: 10.1128/JVI.01815-18
    [62]
    Glowacka I, Bertram S, Müller MA, et al. Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the humoral immune response[J]. J Virol, 2011, 85(9): 4122−4134. doi: 10.1128/JVI.02232-10
    [63]
    Li WH, Moore MJ, Vasilieva N, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus[J]. Nature, 2003, 426(6965): 450−454. doi: 10.1038/nature02145
    [64]
    Moore MJ, Dorfman T, Li WH, et al. Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2[J]. J Virol, 2004, 78(19): 10628−10635. doi: 10.1128/JVI.78.19.10628-10635.2004
    [65]
    Hofmann H, Hattermann K, Marzi A, et al. S protein of severe acute respiratory syndrome-associated coronavirus mediates entry into hepatoma cell lines and is targeted by neutralizing antibodies in infected patients[J]. J Virol, 2004, 78(12): 6134−6142. doi: 10.1128/JVI.78.12.6134-6142.2004
    [66]
    Jiang F, Yang JM, Zhang Y, et al. Angiotensin-converting enzyme 2 and angiotensin 1-7: novel therapeutic targets[J]. Nat Rev Cardiol, 2014, 11(7): 413−426. doi: 10.1038/nrcardio.2014.59
    [67]
    Wysocki J, Schulze A, Batlle D. Novel variants of angiotensin converting enzyme-2 of shorter molecular size to target the kidney renin angiotensin system[J]. Biomolecules, 2019, 9(12): 886. doi: 10.3390/biom9120886
    [68]
    Millet JK, Tang T, Nathan L, et al. Production of pseudotyped particles to study highly pathogenic coronaviruses in a biosafety level 2 setting[J]. J Vis Exp, 2019(145): e59010. doi: 10.3791/59010
    [69]
    Simmons G, Reeves JD, Rennekamp AJ, et al. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry[J]. Proc Natl Acad Sci USA, 2004, 101(12): 4240−4245. doi: 10.1073/pnas.0306446101
    [70]
    Inoue Y, Tanaka N, Tanaka Y, et al. Clathrin-dependent entry of severe acute respiratory syndrome coronavirus into target cells expressing ACE2 with the cytoplasmic tail deleted[J]. J Virol, 2007, 81(16): 8722−8729. doi: 10.1128/JVI.00253-07
    [71]
    Ohkuma S, Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents[J]. Proc Natl Acad Sci USA, 1978, 75(7): 3327−3331. doi: 10.1073/pnas.75.7.3327
    [72]
    Mingo RM, Simmons JA, Shoemaker CJ, et al. Ebola virus and severe acute respiratory syndrome coronavirus display late cell entry kinetics: evidence that transport to NPC1+ endolysosomes is a rate-defining step[J]. J Virol, 2015, 89(5): 2931−2943. doi: 10.1128/JVI.03398-14
    [73]
    Ren XF, Glende J, Al-Falah M, et al. Analysis of ACE2 in polarized epithelial cells: surface expression and function as receptor for severe acute respiratory syndrome-associated coronavirus[J]. J Gen Virol, 2006, 87(Pt 6): 1691−1695. doi: 10.1099/vir.0.81749-0
    [74]
    Tseng CTK, Tseng J, Perrone L, et al. Apical entry and release of severe acute respiratory syndrome-associated coronavirus in polarized Calu-3 lung epithelial cells[J]. J Virol, 2005, 79(15): 9470−9479. doi: 10.1128/JVI.79.15.9470-9479.2005
    [75]
    Kawase M, Shirato K, Van Der Hoek L, et al. Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry[J]. J Virol, 2012, 86(12): 6537−6545. doi: 10.1128/JVI.00094-12
    [76]
    Wang HL, Yang P, Liu KT, et al. SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway[J]. Cell Res, 2008, 18(2): 290−301. doi: 10.1038/cr.2008.15
    [77]
    Lambert DW, Clarke NE, Hooper NM, et al. Calmodulin interacts with angiotensin-converting enzyme-2 (ACE2) and inhibits shedding of its ectodomain[J]. FEBS Lett, 2008, 582(2): 385−390. doi: 10.1016/j.febslet.2007.11.085
    [78]
    Lai ZW, Lew RA, Yarski MA, et al. The identification of a calmodulin-binding domain within the cytoplasmic tail of angiotensin-converting enzyme-2[J]. Endocrinology, 2009, 150(5): 2376−2381. doi: 10.1210/en.2008-1274
    [79]
    Myers MD, Ryazantsev S, Hicke L, et al. Calmodulin promotes N-BAR domain-mediated membrane constriction and endocytosis[J]. Dev Cell, 2016, 37(2): 162−173. doi: 10.1016/j.devcel.2016.03.012
    [80]
    Li GM, Li YG, Yamate M, et al. Lipid rafts play an important role in the early stage of severe acute respiratory syndrome-coronavirus life cycle[J]. Microbes Infect, 2007, 9(1): 96−102. doi: 10.1016/j.micinf.2006.10.015
    [81]
    Wang SX, Guo F, Liu KT, et al. Endocytosis of the receptor-binding domain of SARS-CoV spike protein together with virus receptor ACE2[J]. Virus Res, 2008, 136(1-2): 8−15. doi: 10.1016/j.virusres.2008.03.004
    [82]
    Warner FJ, Lew RA, Smith AI, et al. Angiotensin-converting enzyme 2 (ACE2), but not ACE, is preferentially localized to the apical surface of polarized kidney cells[J]. J Biol Chem, 2005, 280(47): 39353−39362. doi: 10.1074/jbc.M508914200
    [83]
    Lu YN, Liu DX, Tam JP. Lipid rafts are involved in SARS-CoV entry into Vero E6 cells[J]. Biochem Biophys Res Commun, 2008, 369(2): 344−349. doi: 10.1016/j.bbrc.2008.02.023
    [84]
    Glende J, Schwegmann-Wessels C, Al-Falah M, et al. Importance of cholesterol-rich membrane microdomains in the interaction of the S protein of SARS-coronavirus with the cellular receptor angiotensin-converting enzyme 2[J]. Virology, 2008, 381(2): 215−221. doi: 10.1016/j.virol.2008.08.026
    [85]
    Millet JK, Whittaker GR. Physiological and molecular triggers for SARS-CoV membrane fusion and entry into host cells[J]. Virology, 2018, 517: 3−8. doi: 10.1016/j.virol.2017.12.015
    [86]
    Freeman MC, Peek CT, Becker MM, et al. Coronaviruses induce entry-independent, continuous macropinocytosis[J]. mBio, 2014, 5(4): e01340−14.
    [87]
    Yang N, Ma P, Lang JS, et al. Phosphatidylinositol 4-kinase IIIβ is required for severe acute respiratory syndrome coronavirus spike-mediated cell entry[J]. J Biol Chem, 2012, 287(11): 8457−8467. doi: 10.1074/jbc.M111.312561
    [88]
    Yu YTC, Chien SC, Chen IY, et al. Surface vimentin is critical for the cell entry of SARS-CoV[J]. J Biomed Sci, 2016, 23: 14. doi: 10.1186/s12929-016-0234-7
    [89]
    Dyall J, Coleman CM, Hart BJ, et al. Repurposing of clinically developed drugs for treatment of Middle East respiratory syndrome coronavirus infection[J]. Antimicrob Agents Chemother, 2014, 58(8): 4885−4893. doi: 10.1128/AAC.03036-14
    [90]
    Coleman CM, Sisk JM, Mingo RM, et al. Abelson kinase inhibitors are potent inhibitors of severe acute respiratory syndrome coronavirus and middle east respiratory syndrome coronavirus fusion[J]. J Virol, 2016, 90(19): 8924−8933. doi: 10.1128/JVI.01429-16
    [91]
    Chen IY, Chang SC, Wu HY, et al. Upregulation of the chemokine (C-C motif) ligand 2 via a severe acute respiratory syndrome coronavirus spike-ACE2 signaling pathway[J]. J Virol, 2010, 84(15): 7703−7712. doi: 10.1128/JVI.02560-09
    [92]
    Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor[J]. Cell, 2020, 181(2): 271−280.e8. doi: 10.1016/j.cell.2020.02.052
    [93]
    Liu J, Cao R, Xu M, et al. Hydroxychloroquine, a less toxic derivative of chloroquine, is effective in inhibiting SARS-CoV-2 infection in vitro[J]. Cell Discov, 2020, 6: 16.
    [94]
    Wang K, Chen W, Zhang Z, et al. CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells[J]. Signal Transduct Target Ther, 2020, 5(1): 283. doi: 10.1038/s41392-020-00426-x
    [95]
    Rodon J, Noguera-Julian M, Erkizia I, et al. Search for SARS-CoV-2 inhibitors in currently approved drugs to tackle COVID-19 pandemia[J]. bioRxiv, 2020.
    [96]
    Phonphok Y, Rosenthal KS. Stabilization of clathrin coated vesicles by amantadine, tromantadine and other hydrophobic amines[J]. FEBS Lett, 1991, 281(1-2): 188−190. doi: 10.1016/0014-5793(91)80390-O
    [97]
    Bayati A, Kumar R, Francis V, et al. SARS-CoV-2 infects cells after viral entry via clathrin-mediated endocytosis[J]. J Biol Chem, 2021, 296: 100306. doi: 10.1016/j.jbc.2021.100306
    [98]
    Matsuyama S, Nao N, Shirato K, et al. Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells[J]. Proc Natl Acad Sci USA, 2020, 117(13): 7001−7003. doi: 10.1073/pnas.2002589117
    [99]
    Shang J, Wan YS, Luo CM, et al. Cell entry mechanisms of SARS-CoV-2[J]. Proc Natl Acad Sci USA, 2020, 117(21): 11727−11734. doi: 10.1073/pnas.2003138117
    [100]
    Bian HJ, Zheng ZH, Wei D, et al. Meplazumab treats COVID-19 pneumonia: an open-labelled, concurrent controlled add-on clinical trial[EB/OL]. bioRxiv, 2020.
    [101]
    Ulrich H, Pillat MM. CD147 as a target for COVID-19 treatment: suggested effects of azithromycin and stem cell engagement[J]. Stem Cell Rev Rep, 2020, 16(3): 434−440. doi: 10.1007/s12015-020-09976-7
    [102]
    Amraei R, Yin WQ, Napoleon MA, et al. CD209L/L-SIGN and CD209/DC-SIGN act as receptors for SARS-CoV-2 and are differentially expressed in lung and kidney epithelial and endothelial cells[EB/OL]. bioRxiv, 2020, doi: 10.1101/2020.06.22.165803.
    [103]
    De Vries E, Tscherne DM, Wienholts MJ, et al. Dissection of the influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway[J]. PLoS Pathog, 2011, 7(3): e1001329. doi: 10.1371/journal.ppat.1001329
    [104]
    Kälin S, Amstutz B, Gastaldelli M, et al. Macropinocytotic uptake and infection of human epithelial cells with species B2 adenovirus type 35[J]. J Virol, 2010, 84(10): 5336−5350. doi: 10.1128/JVI.02494-09
    [105]
    Coutard B, Valle C, De Lamballerie X, et al. The spike glycoprotein of the new coronavirus 2019-nCoV contains a furin-like cleavage site absent in CoV of the same clade[J]. Antiviral Res, 2020, 176: 104742. doi: 10.1016/j.antiviral.2020.104742
    [106]
    Braun E, Sauter D. Furin-mediated protein processing in infectious diseases and cancer[J]. Clin Transl Immunol, 2019, 8(8): e1073.
    [107]
    Walls AC, Park YJ, Tortorici MA, et al. Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein[J]. Cell, 2020, 181(2): 281−292.e6. doi: 10.1016/j.cell.2020.02.058
    [108]
    Hoffmann M, Kleine-Weber H, Pöhlmann S. A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells[J]. Mol Cell, 2020, 78(4): 779−784.e5. doi: 10.1016/j.molcel.2020.04.022
    [109]
    Millet JK, Whittaker GR. Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein[J]. Proc Natl Acad Sci USA, 2014, 111(42): 15214−15219. doi: 10.1073/pnas.1407087111
    [110]
    Cantuti-Castelvetri L, Ojha R, Pedro LD, et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity[J]. Science, 2020, 370(6518): 856−860. doi: 10.1126/science.abd2985
    [111]
    Teesalu T, Sugahara KN, Kotamraju VR, et al. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration[J]. Proc Natl Acad Sci USA, 2009, 106(38): 16157−16162. doi: 10.1073/pnas.0908201106
    [112]
    Daly JL, Simonetti B, Klein K, et al. Neuropilin-1 is a host factor for SARS-CoV-2 infection[J]. Science, 2020, 370(6518): 861−865. doi: 10.1126/science.abd3072
    [113]
    Moutal A, Martin LF, Boinon L, et al. SARS-CoV-2 Spike protein co-opts VEGF-A/Neuropilin-1 receptor signaling to induce analgesia[J]. PAIN, 2021, 162(1): 243−252. doi: 10.1097/j.pain.0000000000002097
    [114]
    Pang HB, Braun GB, Friman T, et al. An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability[J]. Nat Commun, 2014, 5: 4904. doi: 10.1038/ncomms5904
    [115]
    Palm W, Park Y, Wright K, et al. The utilization of extracellular proteins as nutrients is suppressed by mTORC1[J]. Cell, 2015, 162(2): 259−270. doi: 10.1016/j.cell.2015.06.017
    [116]
    Tugizov SM, Herrera R, Palefsky JM. Epstein-Barr virus transcytosis through polarized oral epithelial cells[J]. J Virol, 2013, 87(14): 8179−8194. doi: 10.1128/JVI.00443-13
    [117]
    Wang HB, Zhang H, Zhang JP, et al. Neuropilin 1 is an entry factor that promotes EBV infection of nasopharyngeal epithelial cells[J]. Nat Commun, 2015, 6: 6240. doi: 10.1038/ncomms7240
    [118]
    Kang YL, Chou YY, Rothlauf PW, et al. Inhibition of PIKfyve kinase prevents infection by Zaire ebolavirus and SARS-CoV-2[J]. Proc Natl Acad Sci USA, 2020, 117(34): 20803−20813. doi: 10.1073/pnas.2007837117
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)

    Article Metrics

    Article views (114) PDF downloads(6) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return