Pathophysiological Consequences of Calcium-Conducting Viroporins

Literature Cited

1. Carrasco L. 1.  1978. Membrane leakiness after viral infection and a new approach to the development of antiviral agents. Nature 272:694–99 [Google Scholar]
2. Carrasco L, Perez L, Irurzun A, Lama J, Martinez-Abarca F. 2.  et al. 1993. Modification of membrane permeability by animal viruses. NATO Adv. Sci. Inst. Ser. A 240:283–303 [Google Scholar]
3. González ME, Carrasco L. 3.  2003. Viroporins. FEBS Lett. 552:28–34 [Google Scholar]
4. Lama J, Carrasco L. 4.  1992. Expression of poliovirus nonstructural proteins in Escherichia coli cells. Modification of membrane permeability induced by 2B and 3A. J. Biol. Chem. 267:15932–37 [Google Scholar]
5. Pinto LH, Holsinger LJ, Lamb RA. 5.  1992. Influenza virus M2 protein has ion channel activity. Cell 69:517–28 [Google Scholar]
6. Sugrue RJ, Hay AJ. 6.  1991. Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology 180:617–24 [Google Scholar]
7. Guinea R, Carrasco L. 7.  1994. Influenza virus M2 protein modifies membrane permeability in E. coli cells. FEBS Lett. 343:242–46 [Google Scholar]
8. Melton JV, Ewart GD, Weir RC, Board PG, Lee E, Gage PW. 8.  2002. Alphavirus 6K proteins form ion channels. J. Biol. Chem. 277:46923–31 [Google Scholar]
9. Ewart GD, Sutherland T, Gage PW, Cox GB. 9.  1996. The Vpu protein of human immunodeficiency virus type 1 forms cation-selective ion channels. J. Virol. 70:7108–15 [Google Scholar]
10. Nieva JL, Madan V, Carrasco L. 10.  2012. Viroporins: structure and biological functions. Nat. Rev. Microbiol. 10:563–74 [Google Scholar]
11. Giorda KM, Hebert DN. 11.  2013. Viroporins customize host cells for efficient viral propagation. DNA Cell Biol. 32:557–64 [Google Scholar]
12. Wang K, Xie S, Sun B. 12.  2011. Viral proteins function as ion channels. Biochim. Biophys. Acta 1808:510–15 [Google Scholar]
13. Pinto LH, Lamb RA. 13.  2006. The M2 proton channels of influenza A and B viruses. J. Biol. Chem. 281:8997–9000 [Google Scholar]
14. Madan V, Castello A, Carrasco L. 14.  2008. Viroporins from RNA viruses induce caspase-dependent apoptosis. Cell Microbiol. 10:437–51 [Google Scholar]
15. van Kuppeveld FJ, de Jong AS, Melchers WJ, Willems PH. 15.  2005. Enterovirus protein 2B po(u)res out the calcium: a viral strategy to survive?. Trends Microbiol 13:41–44 [Google Scholar]
16. Tian P, Hu Y, Schilling WP, Lindsay DA, Eiden J, Estes MK. 16.  1994. The nonstructural glycoprotein of rotavirus affects intracellular calcium levels. J. Virol. 68:251–57 [Google Scholar]
17. Aldabe R, Irurzun A, Carrasco L. 17.  1997. Poliovirus protein 2BC increases cytosolic free calcium concentrations. J. Virol. 71:6214–17 [Google Scholar]
18. Hyser JM, Collinson-Pautz MR, Utama B, Estes MK. 18.  2010. Rotavirus disrupts calcium homeostasis by NSP4 viroporin activity. mBio 1:e00265–10 [Google Scholar]
19. Lu W, Zheng BJ, Xu K, Schwarz W, Du L. 19.  et al. 2006. Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release. PNAS 103:12540–45 [Google Scholar]
20. Chen CC, Kruger J, Sramala I, Hsu HJ, Henklein P. 20.  et al. 2011. ORF8a of SARS-CoV forms an ion channel: experiments and molecular dynamics simulations. Biochim. Biophys. Acta 1808:572–79 [Google Scholar]
21. González ME, Carrasco L. 21.  2005. Viral proteins that enhance membrane permeability. Protein Rev. 1:79–90 [Google Scholar]
22. Lama J, Carrasco L. 22.  1992. Inducible expression of a toxic poliovirus membrane protein in Escherichia coli: comparative studies using different expression systems based on T7 promoters. Biochem. Biophys. Res. Commun. 188:972–81 [Google Scholar]
23. Taube R, Alhadeff R, Assa D, Krugliak M, Arkin IT. 23.  2014. Bacteria-based analysis of HIV-1 Vpu channel activity. PLOS ONE 9:e105387 [Google Scholar]
24. Agirre A, Barco A, Carrasco L, Nieva JL. 24.  2002. Viroporin-mediated membrane permeabilization: pore formation by nonstructural poliovirus 2B protein. J. Biol. Chem. 277:40434–41 [Google Scholar]
25. Henkel M, Mitzner D, Henklein P, Meyer-Almes FJ, Moroni A. 25.  et al. 2010. The proapoptotic influenza A virus protein PB1-F2 forms a nonselective ion channel. PLOS ONE 5:e11112 [Google Scholar]
26. Hyser JM, Utama B, Crawford SE, Estes MK. 26.  2012. Genetic divergence of rotavirus nonstructural protein 4 results in distinct serogroup-specific viroporin activity and intracellular punctate structure morphologies. J. Virol. 86:4921–34 [Google Scholar]
27. Lin TI, Schroeder C. 27.  2001. Definitive assignment of proton selectivity and attoampere unitary current to the M2 ion channel protein of influenza A virus. J. Virol. 75:3647–56 [Google Scholar]
28. Perez M, Garcia-Barreno B, Melero JA, Carrasco L, Guinea R. 28.  1997. Membrane permeability changes induced in Escherichia coli by the SH protein of human respiratory syncytial virus. Virology 235:342–51 [Google Scholar]
29. St. Gelais C, Tuthill TJ, Clarke DS, Rowlands DJ, Harris M, Griffin S. 29.  2007. Inhibition of hepatitis C virus p7 membrane channels in a liposome-based assay system. Antivir. Res. 76:48–58 [Google Scholar]
30. Li Y, To J, Verdia-Baguena C, Dossena S, Surya W. 30.  et al. 2014. Inhibition of the human respiratory syncytial virus small hydrophobic protein and structural variations in a bicelle environment. J. Virol. 88:11899–914 [Google Scholar]
31. Hyser JM. 31.  2015. Viroporins. Electrophysiology of Unconventional Channels and Pores AH Delcour. Berlin: Springer. In press [Google Scholar]
32. Berridge MJ, Lipp P, Bootman MD. 32.  2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11–21 [Google Scholar]
33. Michelangeli F, Ruiz MC, del Castillo JR, Ludert JE, Liprandi F. 33.  1991. Effect of rotavirus infection on intracellular calcium homeostasis in cultured cells. Virology 181:520–27 [Google Scholar]
34. van Kuppeveld FJ, Hoenderop JG, Smeets RL, Willems PH, Dijkman HB. 34.  et al. 1997. Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. EMBO J 16:3519–32 [Google Scholar]
35. Hyser JM, Utama B, Crawford SE, Broughman JR, Estes MK. 35.  2013. Activation of the endoplasmic reticulum calcium sensor STIM1 and store-operated calcium entry by rotavirus requires NSP4 viroporin activity. J. Virol. 87:13579–88 [Google Scholar]
36. Suzuki T, Orba Y, Okada Y, Sunden Y, Kimura T. 36.  et al. 2010. The human polyoma JC virus agnoprotein acts as a viroporin. PLOS Pathog. 6:e1000801 [Google Scholar]
37. de Jong AS, Visch HJ, de Mattia F, Van Dommelen MM, Swarts HG. 37.  et al. 2006. The coxsackievirus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi. J. Biol. Chem. 281:14144–50 [Google Scholar]
38. Ito M, Yanagi Y, Ichinohe T. 38.  2012. Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLOS Pathog. 8:e1002857 [Google Scholar]
39. Wozniak AL, Griffin S, Rowlands D, Harris M, Yi M. 39.  et al. 2010. Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production. PLOS Pathog. 6e1001087
40. Tian P, Estes MK, Hu Y, Ball JM, Zeng CQ, Schilling WP. 40.  1995. The rotavirus nonstructural glycoprotein NSP4 mobilizes Ca²⁺ from the endoplasmic reticulum. J. Virol. 69:5763–72 [Google Scholar]
41. Ruiz MC, Cohen J, Michelangeli F. 41.  2000. Role of Ca²⁺ in the replication and pathogenesis of rotavirus and other viral infections. Cell Calcium 28:137–49 [Google Scholar]
42. Hyser JM, Estes MK. 42.  2009. Rotavirus vaccines and pathogenesis: 2008. Curr. Opin. Gastroenterol. 25:36–43 [Google Scholar]
43. Aldabe R, Barco A, Carrasco L. 43.  1996. Membrane permeabilization by poliovirus proteins 2B and 2BC. J. Biol. Chem. 271:23134–37 [Google Scholar]
44. Carrasco L. 44.  1995. Modification of membrane permeability by animal viruses. Adv. Virus Res. 45:171–212 [Google Scholar]
45. Irurzun A, Arroyo J, Alvarez A, Carrasco L. 45.  1995. Enhanced intracellular calcium concentration during poliovirus infection. J. Virol. 69:5142–46 [Google Scholar]
46. de Jong AS, de Mattia F, Van Dommelen MM, Lanke K, Melchers WJ. 46.  et al. 2008. Functional analysis of picornavirus 2B proteins: effects on calcium homeostasis and intracellular protein trafficking. J. Virol. 82:3782–90 [Google Scholar]
47. Triantafilou K, Kar S, van Kuppeveld FJ, Triantafilou M. 47.  2013. Rhinovirus-induced calcium flux triggers NLRP3 and NLRC5 activation in bronchial cells. Am. J. Respir. Cell Mol. Biol. 49:923–34 [Google Scholar]
48. Perez JF, Ruiz MC, Chemello ME, Michelangeli F. 48.  1999. Characterization of a membrane calcium pathway induced by rotavirus infection in cultured cells. J. Virol. 73:2481–90 [Google Scholar]
49. Diaz Y, Chemello ME, Pena F, Aristimuno OC, Zambrano JL. 49.  et al. 2008. Expression of nonstructural rotavirus protein NSP4 mimics Ca²⁺ homeostasis changes induced by rotavirus infection in cultured cells. J. Virol. 82:11331–43 [Google Scholar]
50. Zambrano JL, Diaz Y, Pena F, Vizzi E, Ruiz MC. 50.  et al. 2008. Silencing of rotavirus NSP4 or VP7 expression reduces alterations in Ca²⁺ homeostasis induced by infection of cultured cells. J. Virol. 82:5815–24 [Google Scholar]
51. Brunet JP, Cotte-Laffitte J, Linxe C, Quero AM, Geniteau-Legendre M, Servin A. 51.  2000. Rotavirus infection induces an increase in intracellular calcium concentration in human intestinal epithelial cells: role in microvillar actin alteration. J. Virol. 74:2323–32 [Google Scholar]
52. Berkova Z, Morris AP, Estes MK. 52.  2003. Cytoplasmic calcium measurement in rotavirus enterotoxin-enhanced green fluorescent protein (NSP4-EGFP) expressing cells loaded with Fura-2. Cell Calcium 34:55–68 [Google Scholar]
53. Hagbom M, Istrate C, Engblom D, Karlsson T, Rodriguez-Diaz J. 53.  et al. 2011. Rotavirus stimulates release of serotonin (5-HT) from human enterochromaffin cells and activates brain structures involved in nausea and vomiting. PLOS Pathog. 7:e1002115 [Google Scholar]
54. Diaz Y, Pena F, Aristimuno OC, Matteo L, De Agrela M. 54.  et al. 2012. Dissecting the Ca²⁺ entry pathways induced by rotavirus infection and NSP4-EGFP expression in Cos-7 cells. Virus Res. 167:285–96 [Google Scholar]
55. Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK. 55.  1996. Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 272:101–4 [Google Scholar]
56. Dong Y, Zeng CQ, Ball JM, Estes MK, Morris AP. 56.  1997. The rotavirus enterotoxin NSP4 mobilizes intracellular calcium in human intestinal cells by stimulating phospholipase C-mediated inositol 1,4,5-trisphosphate production. PNAS 94:3960–65 [Google Scholar]
57. Morris AP, Scott JK, Ball JM, Zeng CQ, O'Neal WK, Estes MK. 57.  1999. NSP4 elicits age-dependent diarrhea and Ca²⁺ mediated I⁻ influx into intestinal crypts of CF mice. Am. J. Physiol. Gastrointest. Liver Physiol. 277:431–44 [Google Scholar]
58. Seo NS, Zeng CQ, Hyser JM, Utama B, Crawford SE. 58.  et al. 2008. Integrins α1β1 and α2β1 are receptors for the rotavirus enterotoxin. PNAS 105:8811–18 [Google Scholar]
59. Newton K, Meyer JC, Bellamy AR, Taylor JA. 59.  1997. Rotavirus nonstructural glycoprotein NSP4 alters plasma membrane permeability in mammalian cells. J. Virol. 71:9458–65 [Google Scholar]
60. Browne EP, Bellamy AR, Taylor JA. 60.  2000. Membrane-destabilizing activity of rotavirus NSP4 is mediated by a membrane-proximal amphipathic domain. J. Gen. Virol. 81:1955–59 [Google Scholar]
61. van Kuppeveld FJ, Galama JM, Zoll J, van den Hurk PJ, Melchers WJ. 61.  1996. Coxsackie B3 virus protein 2B contains cationic amphipathic helix that is required for viral RNA replication. J. Virol. 70:3876–86 [Google Scholar]
62. Campanella M, de Jong AS, Lanke KW, Melchers WJ, Willems PH. 62.  et al. 2004. The coxsackievirus 2B protein suppresses apoptotic host cell responses by manipulating intracellular Ca²⁺ homeostasis. J. Biol. Chem. 279:18440–50 [Google Scholar]
63. Berkova Z, Crawford SE, Trugnan G, Yoshimori T, Morris AP, Estes MK. 63.  2006. Rotavirus NSP4 induces a novel vesicular compartment regulated by calcium and associated with viroplasms. J. Virol. 80:6061–71 [Google Scholar]
64. Bhowmick R, Halder UC, Chattopadhyay S, Chanda S, Nandi S. 64.  et al. 2012. Rotaviral enterotoxin nonstructural protein 4 targets mitochondria for activation of apoptosis during infection. J. Biol. Chem. 287:35004–20 [Google Scholar]
65. Bugarcic A, Taylor JA. 65.  2006. Rotavirus nonstructural glycoprotein NSP4 is secreted from the apical surfaces of polarized epithelial cells. J. Virol. 80:12343–49 [Google Scholar]
66. Storey SM, Gibbons TF, Williams CV, Parr RD, Schroeder F, Ball JM. 66.  2007. Full-length, glycosylated NSP4 is localized to plasma membrane caveolae by a novel raft isolation technique. J. Virol. 81:5472–83 [Google Scholar]
67. Taylor MP, Kirkegaard K. 67.  2007. Modification of cellular autophagy protein LC3 by poliovirus. J. Virol. 81:12543–53 [Google Scholar]
68. Putney JW Jr. 68.  1986. A model for receptor-regulated calcium entry. Cell Calcium 7:1–12 [Google Scholar]
69. Putney JW Jr. 69.  2004. Store-operated calcium channels: How do we measure them, and why do we care?. Sci. Signal. 2004pe37
70. Smyth JT, Dehaven WI, Jones BF, Mercer JC, Trebak M. 70.  et al. 2006. Emerging perspectives in store-operated Ca²⁺ entry: roles of Orai, Stim and TRP. Biochim. Biophys. Acta 1763:1147–60 [Google Scholar]
71. Soboloff J, Rothberg BS, Madesh M, Gill DL. 71.  2012. STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol. 13:549–65 [Google Scholar]
72. del Castillo JR, Ludert JE, Sanchez A, Ruiz MC, Michelangeli F, Liprandi F. 72.  1991. Rotavirus infection alters Na⁺ and K⁺ homeostasis in MA-104 cells. J. Gen. Virol. 72:541–47 [Google Scholar]
73. Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC, Dormitzer PR. 73.  2009. Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science 324:1444–47 [Google Scholar]
74. Sen A, Sen N, Mackow ER. 74.  2007. The formation of viroplasm-like structures by the rotavirus NSP5 protein is calcium regulated and directed by a C-terminal helical domain. J. Virol. 81:11758–67 [Google Scholar]
75. Sastri NP, Viskovska M, Hyser JM, Tanner MR, Horton LB. 75.  et al. 2014. Structural plasticity of the coiled-coil domain of rotavirus NSP4. J. Virol. 88:13602–12 [Google Scholar]
76. Yang Y, Guo Q, Peng T, Gu Q, Zhao J, Xiong D. 76.  1996. Effect of verapamil on Ca²⁺ influx and CVB3-RNA replication in cultured neonatal rat heart cells infected with CVB3. Chin. Med. Sci. J. 11:89–92 [Google Scholar]
77. Brisac C, Teoule F, Autret A, Pelletier I, Colbere-Garapin F. 77.  et al. 2010. Calcium flux between the endoplasmic reticulum and mitochondrion contributes to poliovirus-induced apoptosis. J. Virol. 84:12226–35 [Google Scholar]
78. Michelangeli F, Liprandi F, Chemello ME, Ciarlet M, Ruiz MC. 78.  1995. Selective depletion of stored calcium by thapsigargin blocks rotavirus maturation but not the cytopathic effect. J. Virol. 69:3838–47 [Google Scholar]
79. Ruiz MC, Aristimuno OC, Diaz Y, Pena F, Chemello ME. 79.  et al. 2007. Intracellular disassembly of infectious rotavirus particles by depletion of Ca²⁺ sequestered in the endoplasmic reticulum at the end of virus cycle. Virus Res. 130:140–50 [Google Scholar]
80. Crawford SE, Hyser JM, Utama B, Estes MK. 80.  2012. Autophagy hijacked through viroporin-activated calcium/calmodulin-dependent kinase kinase-β signaling is required for rotavirus replication. PNAS 109:E3405–13 [Google Scholar]
81. Hagbom M, Sharma S, Lundgren O, Svensson L. 81.  2012. Towards a human rotavirus disease model. Curr. Opin. Virol. 2:408–18 [Google Scholar]
82. Ousingsawat J, Mirza M, Tian Y, Roussa E, Schreiber R. 82.  et al. 2011. Rotavirus toxin NSP4 induces diarrhea by activation of TMEM16A and inhibition of Na⁺ absorption. Pflüg. Arch. 461:579–89 [Google Scholar]
83. Ko EA, Jin BJ, Namkung W, Ma T, Thiagarajah JR, Verkman AS. 83.  2014. Chloride channel inhibition by a red wine extract and a synthetic small molecule prevents rotaviral secretory diarrhoea in neonatal mice. Gut 63:1120–29 [Google Scholar]
84. De Marco G, Bracale I, Buccigrossi V, Bruzzese E, Canani RB. 84.  et al. 2009. Rotavirus induces a biphasic enterotoxic and cytotoxic response in human-derived intestinal enterocytes, which is inhibited by human immunoglobulins. J. Infect. Dis. 200:813–19 [Google Scholar]
85. Murakami T, Ockinger J, Yu J, Byles V, McColl A. 85.  et al. 2012. Critical role for calcium mobilization in activation of the NLRP3 inflammasome. PNAS 109:11282–87 [Google Scholar]
86. Chen IY, Ichinohe T. 86.  2015. Response of host inflammasomes to viral infection. Trends Microbiol. 23:55–63 [Google Scholar]
87. Uchiyama R, Chassaing B, Zhang B, Gewirtz AT. 87.  2015. MyD88-mediated TLR signaling protects against acute rotavirus infection while inflammasome cytokines direct Ab response. Innate Immun. 21:416–28 [Google Scholar]
88. Crawford SE, Estes MK. 88.  2013. Viroporin-mediated calcium-activated autophagy. Autophagy 9:797–98 [Google Scholar]
89. Berkova Z, Crawford SE, Blutt SE, Morris AP, Estes MK. 89.  2007. Expression of rotavirus NSP4 alters the actin network organization through the actin remodeling protein cofilin. J. Virol. 81:3545–53 [Google Scholar]
90. Zambrano JL, Sorondo O, Alcala A, Vizzi E, Diaz Y. 90.  et al. 2012. Rotavirus infection of cells in culture induces activation of RhoA and changes in the actin and tubulin cytoskeleton. PLOS ONE 7:e47612 [Google Scholar]
91. Yang W, McCrae MA. 91.  2012. The rotavirus enterotoxin (NSP4) promotes re-modeling of the intracellular microtubule network. Virus Res. 163:269–74 [Google Scholar]
92. Kang G, Desikan P, Mathan M. 92.  2002. Cytoskeletal changes during poliovirus infection in an intestinal cell line. Indian J. Med. Res. 115:37–45 [Google Scholar]
93. Sobo K, Stuart AD, Rubbia-Brandt L, Brown TD, McKee TA. 93.  2012. Echovirus 11 infection induces dramatic changes in the actin cytoskeleton of polarized Caco-2 cells. J. Gen. Virol. 93:475–87 [Google Scholar]
94. Sanz MA, Perez L, Carrasco L. 94.  1994. Semliki Forest virus 6K protein modifies membrane permeability after inducible expression in Escherichia coli cells. J. Biol. Chem. 269:12106–10 [Google Scholar]
95. Shimbo K, Brassard DL, Lamb RA, Pinto LH. 95.  1995. Viral and cellular small integral membrane proteins can modify ion channels endogenous to Xenopus oocytes. Biophys. J. 69:1819–29 [Google Scholar]
96. Antoine AF, Montpellier C, Cailliau K, Browaeys-Poly E, Vilain JP, Dubuisson J. 96.  2007. The alphavirus 6K protein activates endogenous ionic conductances when expressed in Xenopus oocytes. J. Membr. Biol. 215:37–48 [Google Scholar]
97. Hongo S, Ishii K, Mori K, Takashita E, Muraki Y. 97.  et al. 2004. Detection of ion channel activity in Xenopus laevis oocytes expressing influenza C virus CM2 protein. Arch. Virol. 149:35–50 [Google Scholar]
98. Schubert U, Ferrer-Montiel AV, Oblatt-Montal M, Henklein P, Strebel K, Montal M. 98.  1996. Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells. FEBS Lett. 398:12–18 [Google Scholar]
99. Coady MJ, Daniel NG, Tiganos E, Allain B, Friborg J. 99.  et al. 1998. Effects of Vpu expression on Xenopus oocyte membrane conductance. Virology 244:39–49 [Google Scholar]
100. Suzuki T, Orba Y, Makino Y, Okada Y, Sunden Y. 100.  et al. 2013. Viroporin activity of the JC polyomavirus is regulated by interactions with the adaptor protein complex 3. PNAS 110:18668–73 [Google Scholar]
101. Gibbs JS, Malide D, Hornung F, Bennink JR, Yewdell JW. 101.  2003. The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function. J. Virol. 77:7214–24 [Google Scholar]
102. Chanturiya AN, Basanez G, Schubert U, Henklein P, Yewdell JW, Zimmerberg J. 102.  2004. PB1-F2, an influenza A virus-encoded proapoptotic mitochondrial protein, creates variably sized pores in planar lipid membranes. J. Virol. 78:6304–12 [Google Scholar]
103. Chien TH, Chiang YL, Chen CP, Henklein P, Hanel K. 103.  et al. 2013. Assembling an ion channel: ORF 3a from SARS-CoV. Biopolymers 99:628–35 [Google Scholar]
104. Zhou Y, Frey TK, Yang JJ. 104.  2009. Viral calciomics: interplays between Ca²⁺ and virus. Cell Calcium 46:1–17 [Google Scholar]
105. Ding W, Albrecht B, Kelley RE, Muthusamy N, Kim SJ. 105.  et al. 2002. Human T-cell lymphotropic virus type 1 p12^I expression increases cytoplasmic calcium to enhance the activation of nuclear factor of activated T cells. J. Virol. 76:10374–82 [Google Scholar]
106. Nair A, Michael B, Hiraragi H, Fernandez S, Feuer G. 106.  et al. 2005. Human T lymphotropic virus type 1 accessory protein p12^I modulates calcium-mediated cellular gene expression and enhances p300 expression in T lymphocytes. AIDS Res. Hum. Retrovir. 21:273–84 [Google Scholar]
107. Sanderson CM, Parkinson JE, Hollinshead M, Smith GL. 107.  1996. Overexpression of the vaccinia virus A38L integral membrane protein promotes Ca²⁺ influx into infected cells. J. Virol. 70:905–14 [Google Scholar]
108. Sharon-Friling R, Goodhouse J, Colberg-Poley AM, Shenk T. 108.  2006. Human cytomegalovirus pUL37x1 induces the release of endoplasmic reticulum calcium stores. PNAS 103:19117–22 [Google Scholar]
109. Sharon-Friling R, Shenk T. 109.  2014. Human cytomegalovirus pUL37x1-induced calcium flux activates PKCα, inducing altered cell shape and accumulation of cytoplasmic vesicles. PNAS 111:E1140–48 [Google Scholar]
110. Triantafilou K, Triantafilou M. 110.  2014. Ion flux in the lung: virus-induced inflammasome activation. Trends Microbiol. 22:580–88 [Google Scholar]
111. Mould JA, Paterson RG, Takeda M, Ohigashi Y, Venkataraman P. 111.  et al. 2003. Influenza B virus BM2 protein has ion channel activity that conducts protons across membranes. Dev. Cell 5:175–84 [Google Scholar]
112. Piller SC, Ewart GD, Premkumar A, Cox GB, Gage PW. 112.  1996. Vpr protein of human immunodeficiency virus type 1 forms cation-selective channels in planar lipid bilayers. PNAS 93:111–15 [Google Scholar]
113. González ME, Carrasco L. 113.  1998. The human immunodeficiency virus type 1 Vpu protein enhances membrane permeability. Biochemistry 37:13710–19 [Google Scholar]
114. Silic-Benussi M, Marin O, Biasiotto R, D'Agostino DM, Ciminale V. 114.  2010. Effects of human T-cell leukemia virus type 1 (HTLV-1) p13 on mitochondrial K⁺ permeability: a new member of the viroporin family?. FEBS Lett. 584:2070–75 [Google Scholar]
115. Gan SW, Ng L, Lin X, Gong X, Torres J. 115.  2008. Structure and ion channel activity of the human respiratory syncytial virus (hRSV) small hydrophobic protein transmembrane domain. Protein Sci. 17:813–20 [Google Scholar]
116. Griffin SD, Beales LP, Clarke DS, Worsfold O, Evans SD. 116.  et al. 2003. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, amantadine. FEBS Lett. 535:34–38 [Google Scholar]
117. Griffin SD, Harvey R, Clarke DS, Barclay WS, Harris M, Rowlands DJ. 117.  2004. A conserved basic loop in hepatitis C virus p7 protein is required for amantadine-sensitive ion channel activity in mammalian cells but is dispensable for localization to mitochondria. J. Gen. Virol. 85:451–61 [Google Scholar]
118. Wilson L, McKinlay C, Gage P, Ewart G. 118.  2004. SARS coronavirus E protein forms cation-selective ion channels. Virology 330:322–31 [Google Scholar]
119. Liao Y, Tam JP, Liu DX. 119.  2006. Viroporin activity of SARS-CoV E protein. Adv. Exp. Med. Biol. 581:199–202 [Google Scholar]
120. Zhang R, Wang K, Lv W, Yu W, Xie S. 120.  et al. 2014. The ORF4a protein of human coronavirus 229E functions as a viroporin that regulates viral production. Biochim. Biophys. Acta 1838:1088–95 [Google Scholar]
121. Bodelon G, Labrada L, Martinez-Costas J, Benavente J. 121.  2002. Modification of late membrane permeability in avian reovirus-infected cells: viroporin activity of the S1-encoded nonstructural p10 protein. J. Biol. Chem. 277:17789–96 [Google Scholar]
122. Daniels R, Rusan NM, Wadsworth P, Hebert DN. 122.  2006. SV40 VP2 and VP3 insertion into ER membranes is controlled by the capsid protein VP1: implications for DNA translocation out of the ER. Mol. Cell 24:955–66 [Google Scholar]
123. Daniels R, Sadowicz D, Hebert DN. 123.  2007. A very late viral protein triggers the lytic release of SV40. PLOS Pathog. 3:e98 [Google Scholar]
124. Wetherill LF, Holmes KK, Verow M, Muller M, Howell G. 124.  et al. 2012. High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors. J. Virol. 86:5341–51 [Google Scholar]
125. Joubert DA, Blasdell KR, Audsley MD, Trinidad L, Monaghan P. 125.  et al. 2014. Bovine ephemeral fever rhabdovirus α1 protein has viroporin-like properties and binds importin β1 and importin 7. J. Virol. 88:1591–603 [Google Scholar]
126. Kang M, Moroni A, Gazzarrini S, DiFrancesco D, Thiel G. 126.  et al. 2004. Small potassium ion channel proteins encoded by chlorella viruses. PNAS 101:5318–24 [Google Scholar]
127. Sunstrom NA, Premkumar LS, Premkumar A, Ewart G, Cox GB, Gage PW. 127.  1996. Ion channels formed by NB, an influenza B virus protein. J. Membr. Biol. 150:127–32 [Google Scholar]
128. Snyder JE, Kulcsar KA, Schultz KL, Riley CP, Neary JT. 128.  et al. 2013. Functional characterization of the alphavirus TF protein. J. Virol. 87:8511–23 [Google Scholar]
129. Costin JM, Rausch JM, Garry RF, Wimley WC. 129.  2007. Viroporin potential of the lentivirus lytic peptide (LLP) domains of the HIV-1 gp41 protein. Virol. J. 4:123 [Google Scholar]
130. Takikawa S, Engle RE, Emerson SU, Purcell RH, St. Claire M, Bukh J. 130.  2006. Functional analyses of GB virus B p13 protein: development of a recombinant GB virus B hepatitis virus with a p7 protein. PNAS 103:3345–50 [Google Scholar]
131. Premkumar A, Dong X, Haqshenas G, Gage PW, Gowans EJ. 131.  2006. Amantadine inhibits the function of an ion channel encoded by GB virus B, but fails to inhibit virus replication. Antivir. Ther. 11:289–95 [Google Scholar]
132. Premkumar A, Horan CR, Gage PW. 132.  2005. Dengue virus M protein C-terminal peptide (DVM-C) forms ion channels. J. Membr. Biol. 204:33–38 [Google Scholar]
133. Chang YS, Liao CL, Tsao CH, Chen MC, Liu CI. 133.  et al. 1999. Membrane permeabilization by small hydrophobic nonstructural proteins of Japanese encephalitis virus. J. Virol. 73:6257–64 [Google Scholar]
134. Han Z, Harty RN. 134.  2004. The NS3 protein of bluetongue virus exhibits viroporin-like properties. J. Biol. Chem. 279:43092–97 [Google Scholar]
135. Ivanovic T, Agosto MA, Zhang L, Chandran K, Harrison SC, Nibert ML. 135.  2008. Peptides released from reovirus outer capsid form membrane pores that recruit virus particles. EMBO J 27:1289–98 [Google Scholar]
136. Gallaher WR, Garry RF. 136.  2015. Modeling of the Ebola virus delta peptide reveals a potential lytic sequence motif. Viruses 7:285–305 [Google Scholar]
137. Gros A, Martinez-Quintanilla J, Puig C, Guedan S, Mollevi DG. 137.  et al. 2008. Bioselection of a gain of function mutation that enhances adenovirus 5 release and improves its antitumoral potency. Cancer Res. 68:8928–37 [Google Scholar]