Spike mutations contributing to the altered entry preference of SARS-CoV-2 omicron BA.1 and BA.2

References

• Chan JF, Yuan S, Kok KH, et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet. 2020 Feb 15;395(10223):514–523.
   PubMed Web of Science ®Google Scholar
• Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020 Mar;579(7798):270–273.
   PubMed Web of Science ®Google Scholar
• 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. Emerg Microbes Infect. 2020;9(1):221–236.
   PubMed Web of Science ®Google Scholar
• To KK, Sridhar S, Chiu KH, et al. Lessons learned 1 year after SARS-CoV-2 emergence leading to COVID-19 pandemic. Emerg Microbes Infect. 2021 Dec;10(1):507–535.
   PubMed Web of Science ®Google Scholar
• Viana R, Moyo S, Amoako DG, et al. Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa. Nature. 2022 Mar;603(7902):679–686.
   PubMed Web of Science ®Google Scholar
• Cao Y, Wang J, Jian F, et al. Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. Nature. 2022 Feb;602(7898):657–663.
   PubMed Web of Science ®Google Scholar
• Carreño JM, Alshammary H, Tcheou J, et al. Activity of convalescent and vaccine serum against SARS-CoV-2 Omicron. Nature. 2022 Feb;602(7898):682–688.
   PubMed Web of Science ®Google Scholar
• Cele S, Jackson L, Khoury DS, et al. Omicron extensively but incompletely escapes Pfizer BNT162b2 neutralization. Nature. 2022 Feb;602(7898):654–656.
   PubMed Web of Science ®Google Scholar
• Liu L, Iketani S, Guo Y, et al. Striking antibody evasion manifested by the Omicron variant of SARS-CoV-2. Nature. 2022 Feb;602(7898):676–681.
   PubMed Web of Science ®Google Scholar
• Hachmann NP, Miller J, Collier AY, et al. Neutralization escape by SARS-CoV-2 Omicron subvariants BA.2.12.1, BA.4, and BA.5. N Engl J Med. 2022 Jul 7;387(1):86–88.
   PubMed Web of Science ®Google Scholar
• Arora P, Kempf A, Nehlmeier I, et al. Augmented neutralisation resistance of emerging omicron subvariants BA.2.12.1, BA.4, and BA.5. Lancet Infect Dis. 2022 Aug;22(8):1117–1118.
   PubMed Web of Science ®Google Scholar
• Shuai H, Chan JF, Hu B, et al. Attenuated replication and pathogenicity of SARS-CoV-2 B.1.1.529 Omicron. Nature. 2022 Mar;603(7902):693–699.
   PubMed Web of Science ®Google Scholar
• Halfmann PJ, Iida S, Iwatsuki-Horimoto K, et al. SARS-CoV-2 Omicron virus causes attenuated disease in mice and hamsters. Nature. 2022 Mar;603(7902):687–692.
   PubMed Web of Science ®Google Scholar
• Suzuki R, Yamasoba D, Kimura I, et al. Attenuated fusogenicity and pathogenicity of SARS-CoV-2 Omicron variant. Nature. 2022 Mar;603(7902):700–705.
   PubMed Web of Science ®Google Scholar
• Meng B, Abdullahi A, Ferreira I, et al. Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity. Nature. 2022 Mar;603(7902):706–714.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Tomita K, Hirayama Y, et al. SARS-CoV-2 Omicron spike H655Y mutation is responsible for enhancement of the endosomal entry pathway and reduction of cell surface entry pathways. bioRxiv. 2022:2022.03.21.485084.
   Google Scholar
• Peacock TP, Brown JC, Zhou J, et al. The altered entry pathway and antigenic distance of the SARS-CoV-2 Omicron variant map to separate domains of spike protein. bioRxiv. 2022:2021.12.31.474653.
   Google Scholar
• Zhao H, Lu L, Peng Z, et al. SARS-CoV-2 Omicron variant shows less efficient replication and fusion activity when compared with Delta variant in TMPRSS2-expressed cells. Emerg Microbes Infect. 2022 Dec;11(1):277–283.
   PubMed Web of Science ®Google Scholar
• Yamasoba D, Kimura I, Nasser H, et al. Virological characteristics of the SARS-CoV-2 Omicron BA.2 spike. Cell. 2022 Jun 9;185(12):2103–2115.e19.
   PubMed Web of Science ®Google Scholar
• Uraki R, Kiso M, Iida S, et al. Characterization and antiviral susceptibility of SARS-CoV-2 Omicron BA.2. Nature. 2022 Jul;607(7917):119–127.
   PubMed Web of Science ®Google Scholar
• Kimura I, Yamasoba D, Tamura T, et al. Virological characteristics of the novel SARS-CoV-2 Omicron variants including BA.2.12.1, BA.4 and BA.5. bioRxiv. 2022:2022.05.26.493539.
   Google Scholar
• Qu P, Faraone JN, Evans JP, et al. Differential evasion of delta and omicron immunity and enhanced fusogenicity of SARS-CoV-2 Omicron BA.4/5 and BA.2.12.1 Subvariants. bioRxiv. 2022:2022.05.16.492158.
   Google Scholar
• Lu L, Mok BW, Chen LL, et al. Neutralization of SARS-CoV-2 Omicron variant by sera from BNT162b2 or Coronavac vaccine recipients. Clin Infect Dis. 2021 Dec 16;75(1):e822–e826.
   Web of Science ®Google Scholar
• Chu H, Chan JF, Yuen TT, et al. Comparative tropism, replication kinetics, and cell damage profiling of SARS-CoV-2 and SARS-CoV with implications for clinical manifestations, transmissibility, and laboratory studies of COVID-19: an observational study. Lancet Microbe. 2020 May;1(1):e14–e23.
   PubMedGoogle Scholar
• Chu H, Hu B, Huang X, et al. Host and viral determinants for efficient SARS-CoV-2 infection of the human lung. Nat Commun. 2021 Jan 8;12(1):134.
   PubMed Web of Science ®Google Scholar
• Zhang BZ, Shuai H, Gong HR, et al. Bacillus Calmette-Guérin-induced trained immunity protects against SARS-CoV-2 challenge in K18-hACE2 mice. JCI Insight. 2022 Jun 8;7(11):e157393.
   PubMed Web of Science ®Google Scholar
• Chu H, Hou Y, Yang D, et al. Coronaviruses exploit a host cysteine-aspartic protease for replication. Nature. 2022 Aug 3. doi:10.1038/s41586-022-05148-4.
   Web of Science ®Google Scholar
• Yuen TT, Chan JF, Yan B, et al. Targeting ACLY efficiently inhibits SARS-CoV-2 replication. Int J Biol Sci. 2022;18(12):4714–4730.
   PubMed Web of Science ®Google Scholar
• Shuai H, Chan JF, Yuen TT, et al. Emerging SARS-CoV-2 variants expand species tropism to murines. EBioMedicine. 2021 Nov;73:103643.
   PubMed Web of Science ®Google Scholar
• 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. Mol Cell. 2020 May 21;78(4):779–784.e5.
   PubMed Web of Science ®Google Scholar
• Beumer J, Geurts MH, Lamers MM, et al. A CRISPR/Cas9 genetically engineered organoid biobank reveals essential host factors for coronaviruses. Nat Commun. 2021 Sep 17;12(1):5498.
   PubMed Web of Science ®Google Scholar
• Ou X, Liu Y, Lei X, et al. Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV. Nat Commun. 2020 Mar 27;11(1):1620.
   PubMed Web of Science ®Google Scholar
• Koch J, Uckeley ZM, Doldan P, et al. TMPRSS2 expression dictates the entry route used by SARS-CoV-2 to infect host cells. EMBO J. 2021 Aug 16;40(16):e107821.
   PubMed Web of Science ®Google Scholar
• Du X, Tang H, Gao L, et al. Omicron adopts a different strategy from Delta and other variants to adapt to host. Signal Transduct Target Ther. 2022 Feb 10;7(1):45.
   PubMed Web of Science ®Google Scholar
• Poston D, Weisblum Y, Hobbs A, et al. VPS29 exerts opposing effects on endocytic viral entry. mBio. 2022 Apr 26;13(2):e0300221.
   PubMed Web of Science ®Google Scholar
• Mlcochova P, Kemp SA, Dhar MS, et al. SARS-CoV-2 B.1.617.2 Delta variant replication and immune evasion. Nature. 2021 Nov;599(7883):114–119.
   PubMed Web of Science ®Google Scholar
• Liu Y, Liu J, Johnson BA, et al. Delta spike P681R mutation enhances SARS-CoV-2 fitness over Alpha variant. Cell Rep. 2022 May 17;39(7):110829.
   PubMed Web of Science ®Google Scholar
• Saito A, Irie T, Suzuki R, et al. Enhanced fusogenicity and pathogenicity of SARS-CoV-2 Delta P681R mutation. Nature. 2022 Feb;602(7896):300–306.
   PubMed Web of Science ®Google Scholar
• Neerukonda SN, Vassell R, Lusvarghi S, et al. SARS-CoV-2 delta variant displays moderate resistance to neutralizing antibodies and spike protein properties of higher soluble ACE2 sensitivity, enhanced cleavage and fusogenic activity. Viruses. 2021 Dec 11;13(12).
   PubMed Web of Science ®Google Scholar
• Johnson BA, Xie X, Bailey AL, et al. Loss of furin cleavage site attenuates SARS-CoV-2 pathogenesis. Nature. 2021 Mar;591(7849):293–299.
   PubMed Web of Science ®Google Scholar
• Peacock TP, Goldhill DH, Zhou J, et al. The furin cleavage site in the SARS-CoV-2 spike protein is required for transmission in ferrets. Nat Microbiol. 2021 Jul;6(7):899–909.
   PubMed Web of Science ®Google Scholar
• Walls AC, Park YJ, Tortorici MA, et al. Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell. 2020 Apr 16;181(2):281–292.e6.
   PubMed Web of Science ®Google Scholar
• 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. Antiviral Res. 2020 Apr;176:104742.
   PubMed Web of Science ®Google Scholar
• Meng B, Kemp SA, Papa G, et al. Recurrent emergence of SARS-CoV-2 spike deletion H69/V70 and its role in the Alpha variant B.1.1.7. Cell Rep. 2021 Jun 29;35(13):109292.
   PubMed Web of Science ®Google Scholar
• Kimura I, Yamasoba D, Nasser H, et al. SARS-CoV-2 spike S375F mutation characterizes the Omicron BA.1 variant. bioRxiv. 2022:2022.04.03.486864.
   Google Scholar
• Meng B, Datir R, Choi J, et al. SARS-CoV-2 spike n-terminal domain modulates TMPRSS2-dependent viral entry and fusogenicity. bioRxiv. 2022:2022.05.07.491004.
   Google Scholar
• Pastorio C, Zech F, Noettger S, et al. Determinants of spike infectivity, processing, and neutralization in SARS-CoV-2 Omicron subvariants BA.1 and BA.2. Cell Host Microbe. 2022 Jul 18;S1931-3128(22)00352-3. doi:10.1016/j.chom.2022.07.006.
   PubMed Web of Science ®Google Scholar
• Ren W, Ju X, Gong M, et al. Characterization of SARS-CoV-2 variants B.1.617.1 (Kappa), B.1.617.2 (Delta), and B.1.618 by cell entry and immune evasion. mBio. 2022 Apr 26;13(2):e0009922.
   PubMed Web of Science ®Google Scholar
• Kamiyama D, Sekine S, Barsi-Rhyne B, et al. Versatile protein tagging in cells with split fluorescent protein. Nat Commun. 2016 Mar 18;7:11046.
   PubMed Web of Science ®Google Scholar
• Buchrieser J, Dufloo J, Hubert M, et al. Syncytia formation by SARS-CoV-2-infected cells. Embo J. 2021 Feb 1;40(3):e107405.
   PubMed Web of Science ®Google Scholar
• Hoffmann M, Hofmann-Winkler H, Smith JC, et al. Camostat mesylate inhibits SARS-CoV-2 activation by TMPRSS2-related proteases and its metabolite GBPA exerts antiviral activity. EBioMedicine. 2021 Mar;65:103255.
   PubMed Web of Science ®Google Scholar
• Laporte M, Raeymaekers V, Van Berwaer R, et al. The SARS-CoV-2 and other human coronavirus spike proteins are fine-tuned towards temperature and proteases of the human airways. PLoS Pathog. 2021 Apr;17(4):e1009500.
   PubMed Web of Science ®Google Scholar
• Kishimoto M, Uemura K, Sanaki T, et al. TMPRSS11D and TMPRSS13 activate the SARS-CoV-2 spike protein. Viruses. 2021 Feb 28;13(3).
   PubMed Web of Science ®Google Scholar
• Bestle D, Heindl MR, Limburg H, et al. TMPRSS2 and furin are both essential for proteolytic activation of SARS-CoV-2 in human airway cells. Life Sci Alliance. 2020 Jul 23;3(9):e202000786. doi:10.26508/lsa.202000786.
   PubMed Web of Science ®Google Scholar
• Millet JK, Whittaker GR. Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc Natl Acad Sci USA. 2014 Oct 21;111(42):15214–15219.
   PubMed Web of Science ®Google Scholar
• Park JE, Li K, Barlan A, et al. Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism. Proc Natl Acad Sci USA. 2016 Oct 25;113(43):12262–12267.
   PubMed Web of Science ®Google Scholar
• 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. Cell. 2020 Apr 16;181(2):271–280.e8.
   PubMed Web of Science ®Google Scholar
• Zang R, Gomez Castro MF, McCune BT, et al. TMPRSS2 and TMPRSS4 promote SARS-CoV-2 infection of human small intestinal enterocytes. Sci Immunol. 2020 May 13;5(47):eabc3582. doi:10.1126/sciimmunol.abc3582.
   PubMed Web of Science ®Google Scholar
• Escalera A, Gonzalez-Reiche AS, Aslam S, et al. Mutations in SARS-CoV-2 variants of concern link to increased spike cleavage and virus transmission. Cell Host Microbe. 2022 Mar 9;30(3):373–387.e7.
   PubMed Web of Science ®Google Scholar