Volume 42 Issue 2
Mar.  2021
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Yun Zhang, Qi-Quan Wang, Zhong Zhao, Cheng-Jie Deng. Animal secretory endolysosome channel discovery. Zoological Research, 2021, 42(2): 141-152. doi: 10.24272/j.issn.2095-8137.2020.358
Citation: Yun Zhang, Qi-Quan Wang, Zhong Zhao, Cheng-Jie Deng. Animal secretory endolysosome channel discovery. Zoological Research, 2021, 42(2): 141-152. doi: 10.24272/j.issn.2095-8137.2020.358

Animal secretory endolysosome channel discovery

doi: 10.24272/j.issn.2095-8137.2020.358
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (31572268, U1602225, 31872226) and Yunling Scholar Program to Y.Z.
More Information
  • Corresponding author: E-mail: zhangy@mail.kiz.ac.cn
  • Received Date: 2020-12-09
  • Accepted Date: 2021-01-29
  • Available Online: 2021-02-01
  • Publish Date: 2021-03-18
  • Secretory pore-forming proteins (PFPs) have been identified in organisms from all kingdoms of life. Our studies with the toad species Bombina maxima found an interaction network among aerolysin family PFPs (af-PFPs) and trefoil factors (TFFs). As a toad af-PFP, BmALP1 can be reversibly regulated between active and inactive forms, with its paralog BmALP3 acting as a negative regulator. BmALP1 interacts with BmTFF3 to form a cellular active complex called βγ-CAT. This PFP complex is characterized by acting on endocytic pathways and forming pores on endolysosomes, including stimulating cell macropinocytosis. In addition, cell exocytosis can be induced and/or modulated in the presence of βγ-CAT. Depending on cell contexts and surroundings, these effects can facilitate the toad in material uptake and vesicular transport, while maintaining mucosal barrier function as well as immune defense. Based on experimental evidence, we hereby propose a secretory endolysosome channel (SELC) pathway conducted by a secreted PFP in cell endocytic and exocytic systems, with βγ-CAT being the first example of a SELC protein. With essential roles in cell interactions and environmental adaptations, the proposed SELC protein pathway should be conserved in other living organisms.
  • #Authors contributed equally to this work
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  • [1]
    Antonescu CN, McGraw TE, Klip A. 2014. Reciprocal regulation of endocytosis and metabolism. Cold Spring Harbor Perspectives in Biology, 6(7): a016964. doi: 10.1101/cshperspect.a016964
    [2]
    Bücker R, Krug SM, Rosenthal R, Günzel D, Fromm A, Zeitz M, et al. 2011. Aerolysin from Aeromonas hydrophila perturbs tight junction integrity and cell lesion repair in intestinal epithelial HT-29/B6 cells. The Journal of Infectious Diseases, 204(8): 1283−1292. doi: 10.1093/infdis/jir504
    [3]
    Banjara S, Suraweera CD, Hinds MG, Kvansakul M. 2020. The Bcl-2 family: ancient origins, conserved structures, and divergent mechanisms. Biomolecules, 10(1): 128. doi: 10.3390/biom10010128
    [4]
    Barbeau TR, Lillywhite HB. 2005. Body wiping behaviors associated with cutaneous lipids in hylid tree frogs of Florida. The Journal of Experimental Biology, 208(Pt 11): 2147−2156.
    [5]
    Broz P, Pelegrín P, Shao F. 2020. The gasdermins, a protein family executing cell death and inflammation. Nature Reviews Immunology, 20(3): 143−157. doi: 10.1038/s41577-019-0228-2
    [6]
    Burggren WW, Warburton S. 2007. Amphibians as animal models for laboratory research in physiology. ILAR Journal, 48(3): 260−269. doi: 10.1093/ilar.48.3.260
    [7]
    Centeno FC, Antoniazzi MM, Andrade DV, Kodama RT, Sciani JM, Pimenta DC, et al. 2015. Anuran skin and basking behavior: the case of the treefrog Bokermannohyla alvarengai (Bokermann, 1956). Journal of Morphology, 276(10): 1172−1182. doi: 10.1002/jmor.20407
    [8]
    Chang CY, Thompson H, Rodman N, Bylander J, Thomas J. 1997. Pathogenic analysis of Aeromonas hydrophila septicemia. Annals of Clinical and Laboratory Science, 27(4): 254−259.
    [9]
    Cirauqui N, Abriata LA, Van Der Goot FG, Dal Peraro M. 2017. Structural, physicochemical and dynamic features conserved within the aerolysin pore-forming toxin family. Scientific Reports, 7(1): 13932. doi: 10.1038/s41598-017-13714-4
    [10]
    Coffman RL, Sher A, Seder RA. 2010. Vaccine adjuvants: putting innate immunity to work. Immunity, 33(4): 492−503. doi: 10.1016/j.immuni.2010.10.002
    [11]
    Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature, 422(6927): 37−44. doi: 10.1038/nature01451
    [12]
    Cossart P, Helenius A. 2014. Endocytosis of viruses and bacteria. Cold Spring Harbor Perspectives in Biology, 6(8): a016972. doi: 10.1101/cshperspect.a016972
    [13]
    Cullen PJ, Steinberg F. 2018. To degrade or not to degrade: mechanisms and significance of endocytic recycling. Nature Reviews Molecular Cell Biology, 19(11): 679−696. doi: 10.1038/s41580-018-0053-7
    [14]
    Dal Peraro M, Van Der Goot FG. 2016. Pore-forming toxins: ancient, but never really out of fashion. Nature Reviews Microbiology, 14(2): 77−92.
    [15]
    Dang LY, Rougé P, Van Damme EJM. 2017. Amaranthin-like proteins with aerolysin domains in plants. Frontiers in Plant Science, 8: 1368. doi: 10.3389/fpls.2017.01368
    [16]
    De Colibus L, Sonnen AFP, Morris KJ, Siebert CA, Abrusci P, Plitzko J, et al. 2012. Structures of lysenin reveal a shared evolutionary origin for pore-forming proteins and its mode of sphingomyelin recognition. Structure, 20(9): 1498−1507. doi: 10.1016/j.str.2012.06.011
    [17]
    Delbridge ARD, Grabow S, Strasser A, Vaux DL. 2016. Thirty years of BCL-2: translating cell death discoveries into novel cancer therapies. Nature Reviews Cancer, 16(2): 99−109. doi: 10.1038/nrc.2015.17
    [18]
    Deng CJ, Liu L, Liu LZ, Wang QQ, Guo XL, Lee WH, et al. 2020. A secreted pore-forming protein modulates cellular endolysosomes to augment antigen presentation. FASEB Journal, 34(10): 13609−13625. doi: 10.1096/fj.202001176R
    [19]
    Doherty GJ, McMahon HT. 2009. Mechanisms of endocytosis. Annual Review of Biochemistry, 78: 857−902.
    [20]
    Donaldson JG, Porat-Shliom N, Cohen LA. 2009. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cellular Signalling, 21(1): 1−6. doi: 10.1016/j.cellsig.2008.06.020
    [21]
    Eltzschig HK, Carmeliet P. 2011. Hypoxia and inflammation. The New England Journal of Medicine, 364(7): 656−665. doi: 10.1056/NEJMra0910283
    [22]
    Fivaz M, Abrami L, Tsitrin Y, Van Der Goot FG. 2001. Aerolysin from Aeromonas hydrophila and related toxins. In: van der Goot FG. Pore-Forming Toxins. Berlin, Heidelberg: Springer, 35−52.
    [23]
    Galinier R, Portela J, Moné Y, Allienne JF, Henri H, Delbecq S, et al. 2013. Biomphalysin, a new β pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni. PLoS Pathogens, 9(3): e1003216. doi: 10.1371/journal.ppat.1003216
    [24]
    Galvin BD, Kim S, Horvitz HR. 2008. Caenorhabditis elegans genes required for the engulfment of apoptotic corpses function in the cytotoxic cell deaths induced by mutations in lin-24 and lin-33. Genetics, 179(1): 403−417. doi: 10.1534/genetics.108.087221
    [25]
    Gao Q, Xiang Y, Chen ZM, Zeng L, Ma XT, Zhang Y. 2011a. βγ-CAT, a non-lens betagamma-crystallin and trefoil factor complex, induces calcium-dependent platelet apoptosis. Thromb Haemost, 105(5): 846−854. doi: 10.1160/TH10-10-0690
    [26]
    Gao Q, Xiang Y, Zeng L, Ma XT, Lee WH, Zhang Y. 2011b. Characterization of the βγ-crystallin domains of βγ-CAT, a non-lens βγ-crystallin and trefoil factor complex, from the skin of the toad Bombina maxima. Biochimie, 93(10): 1865−1872. doi: 10.1016/j.biochi.2011.07.013
    [27]
    Gao ZH, Deng CJ, Xie YY, Guo XL, Wang QQ, Liu LZ, et al. 2019. Pore-forming toxin-like protein complex expressed by frog promotes tissue repair. FASEB Journal, 33(1): 782−795. doi: 10.1096/fj.201800087R
    [28]
    Gu ZZ, Noss EH, Hsu VW, Brenner MB. 2011. Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. Journal of Cell Biology, 193(1): 61−70. doi: 10.1083/jcb.201007003
    [29]
    Guo XL, Liu LZ, Wang QQ, Liang JY, Lee WH, Xiang Y, et al. 2019. Endogenous pore-forming protein complex targets acidic glycosphingolipids in lipid rafts to initiate endolysosome regulation. Communications Biology, 2(1): 59. doi: 10.1038/s42003-019-0304-y
    [30]
    Gurcel L, Abrami L, Girardin S, Tschopp J, Van Der Goot FG. 2006. Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell, 126(6): 1135−1145. doi: 10.1016/j.cell.2006.07.033
    [31]
    Haslam IS, Roubos EW, Mangoni ML, Yoshizato K, Vaudry H, Kloepper JE, et al. 2014. From frog integument to human skin: dermatological perspectives from frog skin biology. Biological Reviews, 89(3): 618−655. doi: 10.1111/brv.12072
    [32]
    He YY, Liu SB, Lee WH, Zhang Y. 2008a. Melanoma cell growth inhibition by βγ-CAT, which is a novel non-lens betagamma-crystallin and trefoil factor complex from frog Bombina maxima skin. Toxicon, 52(2): 341−347.
    [33]
    He YY, Liu SB, Qian JQ, Lee WH, Zhang Y. 2008b. Mechanism of βγ-CAT cell nuclear transportation and selectively killing of tumor cells. Zoological Research, 29(4): 386−398. doi: 10.3724/SP.J.1141.2008.00386
    [34]
    Ho NI, Huis in 'T Veld LGM, Raaijmakers TK, Adema GJ. 2018. Adjuvants enhancing cross-presentation by dendritic cells: the key to more effective vaccines?. Frontiers in Immunology, 9: 2874. doi: 10.3389/fimmu.2018.02874
    [35]
    Jia N, Liu N, Cheng W, Jiang YL, Sun H, Chen LL, et al. 2016. Structural basis for receptor recognition and pore formation of a zebrafish aerolysin-like protein. EMBO Reports, 17(2): 235−248. doi: 10.15252/embr.201540851
    [36]
    Jørgensen CB. 2000. Amphibian respiration and olfaction and their relationships: from Robert Townson (1794) to the present. Biological Reviews of the Cambridge Philosophical Society, 75(3): 297−345. doi: 10.1017/S0006323100005491
    [37]
    Jouette J, Guichet A, Claret SB. 2019. Dynein-mediated transport and membrane trafficking control PAR3 polarised distribution. eLife, 8: e40212. doi: 10.7554/eLife.40212
    [38]
    Klumperman J, Raposo G. 2014. The complex ultrastructure of the endolysosomal system. Cold Spring Harbor Perspectives in Biology, 6(10): a016857. doi: 10.1101/cshperspect.a016857
    [39]
    Kovacs SB, Miao EA. 2017. Gasdermins: effectors of pyroptosis. Trends in Cell Biology, 27(9): 673−684. doi: 10.1016/j.tcb.2017.05.005
    [40]
    Le Droguen PM, Claret S, Guichet A, Brodu V. 2015. Microtubule-dependent apical restriction of recycling endosomes sustains adherens junctions during morphogenesis of the Drosophila tracheal system. Development, 142(2): 363−374. doi: 10.1242/dev.113472
    [41]
    Li SA, Liu L, Guo XL, Zhang YY, Xiang Y, Wang QQ, et al. 2017. Host pore-forming protein complex neutralizes the acidification of endocytic organelles to counteract intracellular pathogens. The Journal of Infectious Diseases, 215(11): 1753−1763. doi: 10.1093/infdis/jix183
    [42]
    Lim JP, Gleeson PA. 2011. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunology & Cell Biology, 89(8): 836−843.
    [43]
    Lindenbergh MFS, Stoorvogel W. 2018. Antigen presentation by extracellular vesicles from professional antigen-presenting cells. Annual Review of Immunology, 36: 435−459. doi: 10.1146/annurev-immunol-041015-055700
    [44]
    Liu LS, Zhao LY, Wang SH, Jiang JP. 2016. Research proceedings on amphibian model organisms. Zoological Research, 37(4): 237−245.
    [45]
    Liu SB, He YY, Zhang Y, Lee WH, Qian JQ, Lai R, et al. 2008. A novel non-lens βγ-crystallin and trefoil factor complex from amphibian skin and its functional implications. PLoS One, 3(3): e1770. doi: 10.1371/journal.pone.0001770
    [46]
    Liu X, Lieberman J. 2020. Knocking 'em dead: pore-forming proteins in immune defense. Annual Review of Immunology, 38: 455−485. doi: 10.1146/annurev-immunol-111319-023800
    [47]
    Llanses Martinez M, Rainero E. 2019. Membrane dynamics in cell migration. Essays in Biochemistry, 63(5): 469−482. doi: 10.1042/EBC20190014
    [48]
    Lukoyanova N, Hoogenboom BW, Saibil HR. 2016. The membrane attack complex, perforin and cholesterol-dependent cytolysin superfamily of pore-forming proteins. Journal of Cell Science, 129(11): 2125−2133. doi: 10.1242/jcs.182741
    [49]
    Magalhães GS, Lopes-Ferreira M, Junqueira-De-Azevedo ILM, Spencer PJ, Araújo MS, Portaro FCV, et al. 2005. Natterins, a new class of proteins with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie, 87(8): 687−699. doi: 10.1016/j.biochi.2005.03.016
    [50]
    Manzano S, Megías Z, Martínez C, García A, Aguado E, Chileh T, et al. 2017. Overexpression of a flower-specific aerolysin-like protein from the dioecious plant Rumex acetosa alters flower development and induces male sterility in transgenic tobacco. The Plant Journal, 89(1): 58−72. doi: 10.1111/tpj.13322
    [51]
    McGonigal R, Barrie JA, Yao DG, McLaughlin M, Cunningham ME, Rowan EG, et al. 2019. Glial sulfatides and neuronal complex gangliosides are functionally interdependent in maintaining myelinating axon integrity. The Journal of Neuroscience, 39(1): 63−77. doi: 10.1523/JNEUROSCI.2095-18.2018
    [52]
    Medzhitov R. 2008. Origin and physiological roles of inflammation. Nature, 454(7203): 428−435. doi: 10.1038/nature07201
    [53]
    Meldolesi J. 2018. Exosomes and ectosomes in intercellular communication. Current Biology, 28(8): R435−R444.
    [54]
    Merle NS, Church SE, Fremeaux-Bacchi V, Roumenina LT. 2015. Complement system part I - molecular mechanisms of activation and regulation. Frontiers in Immunology, 6: 262.
    [55]
    Moreno-Layseca P, Icha J, Hamidi H, Ivaska J. 2019. Integrin trafficking in cells and tissues. Nature Cell Biology, 21(2): 122−132. doi: 10.1038/s41556-018-0223-z
    [56]
    Mukherjee S, Zheng H, Derebe MG, Callenberg KM, Partch CL, Rollins D, et al. 2014. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature, 505(7481): 103−107. doi: 10.1038/nature12729
    [57]
    Ogawa M, Takabatake T, Takahashi TC, Takeshima K. 1997. Metamorphic change in EP37 expression: members of the βγ-crystallin superfamily in newt. Development Genes and Evolution, 206(7): 417−424. doi: 10.1007/s004270050071
    [58]
    Ogawa M, Takahashi TC, Takabatake T, Takeshima K. 1998. Isolation and characterization of a gene expressed mainly in the gastric epithelium, a novel member of the ep37 family that belongs to the βγ-crystallin superfamily. Development, Growth & Differentiation, 40(5): 465−473.
    [59]
    Oggero S, Austin-Williams S, Norling LV. 2019. The contrasting role of extracellular vesicles in vascular inflammation and tissue repair. Frontiers in Pharmacology, 10: 1479. doi: 10.3389/fphar.2019.01479
    [60]
    Omersa N, Podobnik M, Anderluh G. 2019. Inhibition of pore-forming proteins. Toxins, 11(9): 545. doi: 10.3390/toxins11090545
    [61]
    Ouldali H, Sarthak K, Ensslen T, Piguet F, Manivet P, Pelta J, et al. 2020. Electrical recognition of the twenty proteinogenic amino acids using an aerolysin nanopore. Nature Biotechnology, 38(2): 176−181. doi: 10.1038/s41587-019-0345-2
    [62]
    Palm W. 2019. Metabolic functions of macropinocytosis. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1765): 20180285. doi: 10.1098/rstb.2018.0285
    [63]
    Palm W, Thompson CB. 2017. Nutrient acquisition strategies of mammalian cells. Nature, 546(7657): 234−242. doi: 10.1038/nature22379
    [64]
    Pang Y, Li CH, Wang SY, Ba W, Yu T, Pei GY, et al. 2017. A novel protein derived from lamprey supraneural body tissue with efficient cytocidal actions against tumor cells. Cell Communication and Signaling, 15(1): 42. doi: 10.1186/s12964-017-0198-6
    [65]
    Podobnik M, Savory P, Rojko N, Kisovec M, Wood N, Hambley R, et al. 2016. Crystal structure of an invertebrate cytolysin pore reveals unique properties and mechanism of assembly. Nature Communications, 7(1): 11598. doi: 10.1038/ncomms11598
    [66]
    Qian JQ, Liu SB, He YY, Lee WH, Zhang Y. 2008a. Acute toxicity of βγ-CAT, a naturally existing non-lens βγ-crystallin and trefoil factor complex from frog Bombina maxima skin secretions. Toxicon, 52(1): 22−31. doi: 10.1016/j.toxicon.2008.05.007
    [67]
    Qian JQ, Liu SB, He YY, Lee WH, Zhang Y. 2008b. βγ-CAT, a non-lens βγ-crystallin and trefoil factor complex from amphibian skin secretions, caused endothelium-dependent myocardial depression in isolated rabbit hearts. Toxicon, 52(2): 285−292. doi: 10.1016/j.toxicon.2008.05.017
    [68]
    Rawat N, Pumphrey MO, Liu SX, Zhang XF, Tiwari VK, Ando K, et al. 2016. Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nature Genetics, 48(12): 1576−1580. doi: 10.1038/ng.3706
    [69]
    Record M, Silvente-Poirot S, Poirot M, Wakelam MJO. 2018. Extracellular vesicles: lipids as key components of their biogenesis and functions. Journal of Lipid Research, 59(8): 1316−1324. doi: 10.1194/jlr.E086173
    [70]
    Romero M, Keyel M, Shi GL, Bhattacharjee P, Roth R, Heuser JE, et al. 2017. Intrinsic repair protects cells from pore-forming toxins by microvesicle shedding. Cell Death & Differentiation, 24(5): 798−808.
    [71]
    Russell AE, Sneider A, Witwer KW, Bergese P, Bhattacharyya SN, Cocks A, et al. 2019. Biological membranes in EV biogenesis, stability, uptake, and cargo transfer: an ISEV position paper arising from the ISEV membranes and EVs workshop. Journal of Extracellular Vesicles, 8(1): 1684862. doi: 10.1080/20013078.2019.1684862
    [72]
    Sadowski-Fugitt LM, Tracy CR, Christian KA, Williams JB. 2012. Cocoon and epidermis of Australian Cyclorana frogs differ in composition of lipid classes that affect water loss. Physiological and Biochemical Zoology, 85(1): 40−50. doi: 10.1086/663695
    [73]
    Schmidt F, Levin J, Kamp F, Kretzschmar H, Giese A, Bötzel K. 2012. Single-channel electrophysiology reveals a distinct and uniform pore complex formed by α-synuclein oligomers in lipid membranes. PLoS One, 7(8): e42545. doi: 10.1371/journal.pone.0042545
    [74]
    Scita G, Di Fiore PP. 2010. The endocytic matrix. Nature, 463(7280): 464−473. doi: 10.1038/nature08910
    [75]
    Sekizawa Y, Kubo T, Kobayashi H, Nakajima T, Natori S. 1997. Molecular cloning of cDNA for lysenin, a novel protein in the earthworm Eisenia foetida that causes contraction of rat vascular smooth muscle. Gene, 191(1): 97−102. doi: 10.1016/S0378-1119(97)00047-4
    [76]
    Shibata Y, Sano T, Tsuchiya N, Okada R, Mochida H, Tanaka S, et al. 2014. Gene expression and localization of two types of AQP5 in Xenopus tropicalis under hydration and dehydration. American Journal of Physiology Regulatory, Integrative and Comparative Physiology, 307(1): R44−R56. doi: 10.1152/ajpregu.00186.2013
    [77]
    Suzuki M, Shibata Y, Ogushi Y, Okada R. 2015. Molecular machinery for vasotocin-dependent transepithelial water movement in amphibians: aquaporins and evolution. The Biological Bulletin, 229(1): 109−119. doi: 10.1086/BBLv229n1p109
    [78]
    Swanson JA, King JS. 2019. The breadth of macropinocytosis research. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1765): 20180146. doi: 10.1098/rstb.2018.0146
    [79]
    Szczesny P, Iacovache I, Muszewska A, Ginalski K, Van Der Goot FG, Grynberg M. 2011. Extending the aerolysin family: from bacteria to vertebrates. PLoS One, 6(6): e20349. doi: 10.1371/journal.pone.0020349
    [80]
    Tandon P, Conlon F, Furlow JD, Horb ME. 2017. Expanding the genetic toolkit in Xenopus: approaches and opportunities for human disease modeling. Developmental Biology, 426(2): 325−335. doi: 10.1016/j.ydbio.2016.04.009
    [81]
    Tuma PL, Hubbard AL. 2003. Transcytosis: crossing cellular barriers. Physiological Reviews, 83(3): 871−932. doi: 10.1152/physrev.00001.2003
    [82]
    Van Der Goot FG, Hardie KR, Parker MW, Buckley JT. 1994. The C-terminal peptide produced upon proteolytic activation of the cytolytic toxin aerolysin is not involved in channel formation. Journal of Biological Chemistry, 269(48): 30496−30501. doi: 10.1016/S0021-9258(18)43841-0
    [83]
    Van Niel G, D'Angelo G, Raposo G. 2018. Shedding light on the cell biology of extracellular vesicles. Nature Reviews Molecular Cell Biology, 19(4): 213−228. doi: 10.1038/nrm.2017.125
    [84]
    Varga JFA, Bui-Marinos MP, Katzenback BA. 2018. Frog skin innate immune defences: sensing and surviving pathogens. Frontiers in Immunology, 9: 3128.
    [85]
    Wang QQ, Bian XL, Zeng L, Pan F, Liu LZ, Liang JY, et al. 2020. A cellular endolysosome-modulating pore-forming protein from a toad is negatively regulated by its paralog under oxidizing conditions. The Journal of Biological Chemistry, 295(30): 10293−10306. doi: 10.1074/jbc.RA120.013556
    [86]
    Wang Y, Gu LQ, Tian K. 2018. The aerolysin nanopore: from peptidomic to genomic applications. Nanoscale, 10(29): 13857−13866. doi: 10.1039/C8NR04255A
    [87]
    Wu FF, Feng B, Ren Y, Wu D, Chen Y, Huang SF, et al. 2017. A pore-forming protein implements VLR-activated complement cytotoxicity in lamprey. Cell Discovery, 3(1): 17033. doi: 10.1038/celldisc.2017.33
    [88]
    Wu LG, Hamid E, Shin W, Chiang HC. 2014. Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annual Review of Physiology, 76: 301−331. doi: 10.1146/annurev-physiol-021113-170305
    [89]
    Xiang Y, Yan C, Guo XL, Zhou KF, Li SA, Gao Q, et al. 2014. Host-derived, pore-forming toxin-like protein and trefoil factor complex protects the host against microbial infection. Proceedings of the National Academy of Sciences of the United States of America, 111(18): 6702−6707. doi: 10.1073/pnas.1321317111
    [90]
    Yáñez-Mó M, Siljander PRM, Andreu Z, Zavec AB, Borràs FE, Buzas EI, et al. 2015. Biological properties of extracellular vesicles and their physiological functions. Journal of Extracellular Vesicles, 4(1): 27066. doi: 10.3402/jev.v4.27066
    [91]
    Ye CJ. 2020. Identification and Study of Ion Channel Functions of Natural Bioactive Substances. Ph.D. dissertation, The University of Chinese Academy of Sciences, China.
    [92]
    Yokoyama H, Kudo N, Todate M, Shimada Y, Suzuki M, Tamura K. 2018. Skin regeneration of amphibians: a novel model for skin regeneration as adults. Development, Growth & Differentiation, 60(6): 316−325.
    [93]
    Zhang Y. 2015. Why do we study animal toxins?. Zoological Research, 36(4): 183−222.
    [94]
    Zhang Y, Yu GY, Wang YJ, Xiang Y, Gao Q, Jiang P, et al. 2011. Activation of protease-activated receptor (PAR) 1 by frog trefoil factor (TFF) 2 and PAR4 by human TFF2. Cellular and Molecular Life Sciences, 68(22): 3771−3780. doi: 10.1007/s00018-011-0678-6
    [95]
    Zhang YX, Lai R, Lee WH, Zhang Y. 2005. Frog albumin is expressed in skin and characterized as a novel potent trypsin inhibitor. Protein Science, 14(9): 2469−2477. doi: 10.1110/ps.051551105
    [96]
    Zhao F, Yan C, Wang X, Yang Y, Wang GY, Lee WH, et al. 2014. Comprehensive transcriptome profiling and functional analysis of the frog (Bombina maxima) immune system. DNA Research, 21(1): 1−13. doi: 10.1093/dnares/dst035
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