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Journal of General Virology header logo Journal of General Virology

Volume 104, Issue 7

Dengue virus M and E proteins belonging to genotype II (Cosmopolitan) of serotype 2 are influenced by the nature of M residue 36 Open Access

Abstract

Mosquito-borne dengue disease is caused by the dengue virus serotype-1 to serotype-4. The contemporary dengue outbreaks in the southwestern Indian ocean coincided with the widespread of dengue virus serotype 2 genotype II (Cosmopolitan), including epidemic viral strains DES-14 and RUN-18 isolated in Dar es Salaam (Tanzania) in 2014 and La Reunion Island (France) in 2018, respectively. Heterodimeric interaction between prM (intracellular precursor of surface structural M protein) and envelope E proteins is required during the initial stage of dengue virus assembly. Amino acid 127 of DES-14 prM protein (equivalent to M36) has been identified as an infrequent valine whereas RUN-18 has a common isoleucine. In the present study, we examined the effect of M-I36V mutation on the expression of a recombinant RUN-18 E protein co-expressed with prM in human epithelial A549 cells. The M ectodomain of dengue virus serotype 2 embeds a pro-apoptotic peptide referred as DAMP. The impact of M-I36V mutation on the death-promoting capability of DAMP was assessed in A549 cells. We showed that valine at position M36 affects expression of recombinant RUN-18 E protein and potentiates apoptosis-inducing activity of DAMP. We propose that the nature of M residue 36 influences the virological characteristics of dengue 2 M and E proteins belonging to genotype II that contributes to global dengue burden.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): apoptotic viral peptide , arbovirus , dengue 2 virus , E protein , flavivirus , genotype II and M protein
Funding
This study was supported by the:
  • POE FEDER 2014-20 (Award PHYTODENGUE n°RE0028005)
    • Principle Award Recipient: NotApplicable
  • ERDF (Award RUNDENG n°2020640-0022937)
    • Principle Award Recipient: NotApplicable
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-07-12
2025-01-14
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References

  1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW et al. The global distribution and burden of dengue. Nature 2013; 496:504–507 [View Article] [PubMed]
     [Google Scholar]
  2. Messina JP, Brady OJ, Golding N, Kraemer MUG, Wint GRW et al. The current and future global distribution and population at risk of dengue. Nat Microbiol 2019; 4:1508–1515 [View Article] [PubMed]
     [Google Scholar]
  3. WHO Dengue and Severe Dengue; 2022 https://www.who.int/news-room/fact-sheets/detail/dengue-and-severe-dengue
  4. Chawla P, Yadav A, Chawla V. Clinical implications and treatment of dengue. Asian Pac J Trop Med 2014; 7:169–178 [View Article] [PubMed]
     [Google Scholar]
  5. Rodenhuis-Zybert IA, Wilschut J, Smit JM. Dengue virus life cycle: viral and host factors modulating infectivity. Cell Mol Life Sci 2010; 67:2773–2786 [View Article] [PubMed]
     [Google Scholar]
  6. Pierson TC, Kielian M. Flaviviruses: braking the entering. Curr Opin Virol 2013; 3:3–12 [View Article] [PubMed]
     [Google Scholar]
  7. Allison SL, Schalich J, Stiasny K, Mandl CW, Heinz FX. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J Virol 2001; 75:4268–4275 [View Article] [PubMed]
     [Google Scholar]
  8. Mukhopadhyay S, Kuhn RJ, Rossmann MG. A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 2005; 3:13–22 [View Article] [PubMed]
     [Google Scholar]
  9. Murray JM, Aaskov JG, Wright PJ. Processing of the dengue virus type 2 proteins prM and C-prM. J Gen Virol 1993; 74 (Pt 2):175–182 [View Article] [PubMed]
     [Google Scholar]
  10. Li L, Lok S-M, Yu I-M, Zhang Y, Kuhn RJ et al. The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 2008; 319:1830–1834 [View Article] [PubMed]
     [Google Scholar]
  11. Zhang W, Chipman PR, Corver J, Johnson PR, Zhang Y et al. Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat Struct Mol Biol 2003; 10:907–912 [View Article]
     [Google Scholar]
  12. Konishi E, Mason PW. Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein. J Virol 1993; 67:1672–1675 [View Article] [PubMed]
     [Google Scholar]
  13. Lorenz IC, Allison SL, Heinz FX, Helenius A. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J Virol 2002; 76:5480–5491 [View Article] [PubMed]
     [Google Scholar]
  14. Stadler K, Allison SL, Schalich J, Heinz FX. Proteolytic activation of tick-borne encephalitis virus by furin. J Virol 1997; 71:8475–8481 [View Article] [PubMed]
     [Google Scholar]
  15. Zhang X, Ge P, Yu X, Brannan JM, Bi G et al. Cryo-EM structure of the mature dengue virus at 3.5-Å resolution. Nat Struct Mol Biol 2013; 20:105–110 [View Article] [PubMed]
     [Google Scholar]
  16. Catteau A, Kalinina O, Wagner M-C, Deubel V, Courageot M-P et al. Dengue virus M protein contains a proapoptotic sequence referred to as ApoptoM. J Gen Virol 2003; 84:2781–2793 [View Article] [PubMed]
     [Google Scholar]
  17. Catteau A, Roué G, Yuste VJ, Susin SA, Desprès P. Expression of dengue ApoptoM sequence results in disruption of mitochondrial potential and caspase activation. Biochimie 2003; 85:789–793 [View Article] [PubMed]
     [Google Scholar]
  18. de Wispelaere M, Khou C, Frenkiel M-P, Desprès P, Pardigon N et al. A single amino acid substitution in the M protein attenuates Japanese encephalitis virus in mammalian hosts. J Virol 2016; 90:2676–2689 [View Article]
     [Google Scholar]
  19. Basset J, Burlaud-Gaillard J, Feher M, Roingeard P, Rey FA et al. A molecular determinant of West Nile virus secretion and morphology as a target for viral attenuation. J Virol 2020; 94:e00086-20 [View Article] [PubMed]
     [Google Scholar]
  20. Hsieh S-C, Zou G, Tsai W-Y, Qing M, Chang G-J et al. The C-terminal helical domain of dengue virus precursor membrane protein is involved in virus assembly and entry. Virology 2011; 410:170–180 [View Article] [PubMed]
     [Google Scholar]
  21. Yenamandra SP, Koo C, Chiang S, Lim HSJ, Yeo ZY et al. Evolution, heterogeneity and global dispersal of cosmopolitan genotype of Dengue virus type 2. Sci Rep 2021; 11:13496 [View Article] [PubMed]
     [Google Scholar]
  22. Giovanetti M, Pereira LA, Santiago GA, Fonseca V, Mendoza MPG et al. Emergence of dengue virus serotype 2 cosmopolitan genotype, Brazil. Emerg Infect Dis 2022; 28:1725–1727 [View Article]
     [Google Scholar]
  23. Pascalis H, Turpin J, Roche M, Krejbich P, Gadea G et al. The epidemic of Dengue virus type-2 cosmopolitan genotype on Reunion Island relates to its active circulation in the Southwestern Indian Ocean neighboring islands. Heliyon 2019; 5:e01455 [View Article] [PubMed]
     [Google Scholar]
  24. Pascalis H, Biscornet L, Toty C, Hafsia S, Roche M et al. Complete genome sequences of Dengue virus type 2 epidemic strains from Reunion Island and the seychelles. Microbiol Resour Announc 2020; 9:e01443-19 [View Article] [PubMed]
     [Google Scholar]
  25. Vairo F, Mboera LEG, De Nardo P, Oriyo NM, Meschi S et al. Clinical, virologic, and epidemiologic characteristics of Dengue outbreak, Dar es Salaam, Tanzania, 2014. Emerg Infect Dis 2016; 22:895–899 [View Article]
     [Google Scholar]
  26. Santé Publique France Surveillance de la dengue à La Réunion; 2023 https://www.santepubliquefrance.fr/recherche/#search=Dengue%20%C3%A0%20La%20R%C3%A9union&themes=dengue®ions=Oc%C3%A9an%20Indien
  27. Hafsia S, Haramboure M, Wilkinson DA, Baldet T, Yemadje-Menudier L et al. Overview of dengue outbreaks in the southwestern Indian Ocean and analysis of factors involved in the shift toward endemicity in Reunion Island: a systematic review. PLoS Negl Trop Dis 2022; 16:e0010547 [View Article] [PubMed]
     [Google Scholar]
  28. ARS Situation de La Dengue à La Réunion; 2019 https://www.lareunion.ars.sante.fr/point-sur-la-dengue-la-reunion-1
  29. Ogire E, Diaz O, Vidalain P-O, Lotteau V, Desprès P et al. Instability of the NS1 glycoprotein from La Reunion 2018 Dengue 2 virus (Cosmopolitan-1 Genotype) in huh7 cells is due to lysine residues on positions 272 and 324. Int J Mol Sci 2021; 22:1951 [View Article] [PubMed]
     [Google Scholar]
  30. Peng J-G, Wu S-C. Glutamic acid at residue 125 of the prM helix domain interacts with positively charged amino acids in E protein domain II for Japanese encephalitis virus-like-particle production. J Virol 2014; 88:8386–8396 [View Article] [PubMed]
     [Google Scholar]
  31. Vanwalscappel B, Haddad JG, Almokdad R, Decotter J, Gadea G et al. Zika M oligopeptide ZAMP confers cell death-promoting capability to a soluble tumor-associated antigen through caspase-3/7 activation. Int J Mol Sci 2020; 21:9578 [View Article] [PubMed]
     [Google Scholar]
  32. Hsieh S-C, Wu Y-C, Zou G, Nerurkar VR, Shi P-Y et al. Highly conserved residues in the helical domain of dengue virus type 1 precursor membrane protein are involved in assembly, precursor membrane (prM) protein cleavage, and entry. J Biol Chem 2014; 289:33149–33160 [View Article] [PubMed]
     [Google Scholar]
  33. Okamoto T, Suzuki T, Kusakabe S, Tokunaga M, Hirano J et al. Regulation of apoptosis during flavivirus infection. Viruses 2017; 9:243 [View Article] [PubMed]
     [Google Scholar]
  34. Turpin J, El Safadi D, Lebeau G, Krejbich M, Chatelain C et al. Apoptosis during ZIKA virus infection: too soon or too late?. Int J Mol Sci 2022; 23:1287 [View Article] [PubMed]
     [Google Scholar]
  35. Pan Y, Cheng A, Wang M, Yin Z, Jia R. The dual regulation of apoptosis by flavivirus. Front Microbiol 2021; 12:654494 [View Article] [PubMed]
     [Google Scholar]
  36. Johnston JA, Illing ME, Kopito RR. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil Cytoskeleton 2002; 53:26–38 [View Article] [PubMed]
     [Google Scholar]
  37. Egan MJ, McClintock MA, Hollyer IHL, Elliott HL, Reck-Peterson SL. Cytoplasmic dynein is required for the spatial organization of protein aggregates in filamentous fungi. Cell Rep 2015; 11:201–209 [View Article] [PubMed]
     [Google Scholar]
  38. Ripon MKH, Lee H, Dash R, Choi HJ, Oktaviani DF et al. N-acetyl-D-glucosamine kinase binds dynein light chain roadblock 1 and promotes protein aggregate clearance. Cell Death Dis 2020; 11:619 [View Article] [PubMed]
     [Google Scholar]
  39. Pan P, Zhang Q, Liu W, Wang W, Lao Z et al. Dengue virus M protein promotes NLRP3 inflammasome activation to induce vascular leakage in mice. J Virol 2019; 93:e00996-19 [View Article] [PubMed]
     [Google Scholar]
  40. Brown E, Beaumont H, Lefteri D, Bentham M, Foster R et al. Flavivirus membrane (M) proteins as potential ion channel antiviral targets. Access Microbiol 2019; 1: [View Article]
     [Google Scholar]
  41. Zheng A, Yuan F, Kleinfelter LM, Kielian M. A toggle switch controls the low pH-triggered rearrangement and maturation of the dengue virus envelope proteins. Nat Commun 2014; 5:3877 [View Article] [PubMed]
     [Google Scholar]
  42. Aubry F, Nougairède A, de Fabritus L, Querat G, Gould EA et al. Single-stranded positive-sense RNA viruses generated in days using infectious subgenomic amplicons. J Gen Virol 2014; 95:2462–2467 [View Article]
     [Google Scholar]
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Dengue virus M and E proteins belonging to genotype II (Cosmopolitan) of serotype 2 are influenced by the nature of M residue 36
J. Gen. Virol. 104, 001872 (2023); https://doi.org/10.1099/jgv.0.001872
/content/journal/jgv/10.1099/jgv.0.001872
/content/journal/jgv/10.1099/jgv.0.001872
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