Landscape of B Cell Receptor Repertoires in COVID-19 Patients Revealed Through CDR3 Sequencing of Immunoglobulin Heavy and Light Chains

References

• Bieberich F, Vazquez-Lombardi R, Yermanos A, Ehling RA, Mason DM, Wagner B, Kapetanovic E, Di Roberto RB, Weber CR, and Savic M, et al. 2021. A Single-cell atlas of lymphocyte adaptive immune repertoires and transcriptomes reveals age-related differences in convalescent COVID-19 patients. Front Immunol. 12:701085.
   PubMed Web of Science ®Google Scholar
• Blachly JS, Ruppert AS, Zhao W, Long S, Flynn J, Flinn I, Jones J, Maddocks K, Andritsos L, Ghia M, et al. 2015. Immunoglobulin transcript sequence and somatic hypermutation computation from unselected RNA-seq reads in chronic lymphocytic leukemia. Proc Natl Acad Sci USA. 112(14):4322–27.
   PubMedGoogle Scholar
• Bolotin D, Poslavsky S, Mitrophanov I, Shugay M, Mamedov IZ, Putintseva EV, Chudakov DM. 2015. MiXCR: Software for comprehensive adaptive immunity profiling. Nat Methods. 12(5):380–81.
   PubMed Web of Science ®Google Scholar
• Chen W, Zhu Z, Xiao X, Dimitrov DS. 2009. Construction of a human antibody domain (VH) library. Methods Mol Biol. 525:81–99.
   PubMedGoogle Scholar
• Collier DA, Ferreira IATM, Kotagiri P, Datir RP, Lim EY, Touizer E, Meng B, Abdullahi A, Baker S, Dougan G, et al. 2021. Age-Related immune response heterogeneity to SARS-CoV-2 vaccine BNT162b2. Nature. 596(7872):417–22.
   PubMed Web of Science ®Google Scholar
• Coronavirus Resource Center. 2022. [accessed 2022 Mar 7]. https://coronavirus.jhu.edu/map.html.
   Google Scholar
• Cui J-H, Lin KR, Yuan SH, Jin YB, Chen XP, Su XK, Jiang J, Pan YM, Mao SL, Mao XF, et al. 2018. TCR repertoire as a novel indicator for immune monitoring and prognosis assessment of patients with cervical cancer. Front Immunol. 9:2729.
   PubMed Web of Science ®Google Scholar
• Davydov AN, Obraztsova AS, Lebedin MY, Turchaninova MA, Staroverov DB, Merzlyak EM, Sharonov GV, Kladova O, Shugay M, Britanova OV, et al. 2018. Comparative analysis of B-cell receptor repertoires induced by live yellow fever vaccine in young and middle-age donors. Front Immunol. 9:2309.
   PubMedGoogle Scholar
• Defrancesco I, Visentini M, Zibellini S, Minafò YA, Rattotti S, Ferretti VV, Rizzo E, Varettoni M, Frigeni M, Pulsoni A, et al. 2021. Mutational and immunogenetic landscape of HCV -associated B-cell lymphoproliferative disorders. Am J Hematol. 96(6):E210–E214.
   PubMedGoogle Scholar
• Fan X, Liu Z, Poulsen KL, Wu X, Miyata T, Dasarathy S, Rotroff DM, Nagy LE. 2020. Alcohol Consumption is Associated with Poor Prognosis in Obese Patients with COVID-19: a Mendelian Randomization Study using UK Biobank. medRxiv: The preprint server for health sciences. 2020.05.24.20101238. doi:10.1101/2020.11.25.20238915.
   Google Scholar
• Funakoshi Y, Ohji G, Yakushijin K, Ebisawa K, Arakawa Y, Saegusa J, Matsumoto H, Imanishi T, ukuda E, Matsutani T, et al. 2021. Massive surge of mRNA expression of clonal B-cell receptor in patients with COVID-19. Heliyon. 7(8):e07748.
   PubMedGoogle Scholar
• Galson JD, Schaetzle S, Bashford-Rogers Rachael J.M., Raybould Matthew I.J., Kovaltsuk A., Kilpatrick Gavin J, Minter R, Finch Donna K, Dias J, James Louisa K, et al. 2020. Deep sequencing of B cell receptor repertoires from COVID-19 patients reveals strong convergent immune signatures. Front Immunol 11:605170.
   PubMed Web of Science ®Google Scholar
• Giallourakis CC, Franklin A, Guo C, Cheng HL, Yoon HS, Gallagher M, Perlot T, Andzelm M, Murphy AJ, Macdonald LE, et al. 2010. Elements between the IgH variable (V) and diversity (D) clusters influence antisense transcription and lineage-specific V(D)J recombination. Immunol Inflamm. 107(51):22207–12.
   Google Scholar
• Glanville J, Zhai W, Berka J, Telman D, Huerta G, Mehta GR, Ni I, Mei L, Sundar PD, Day GM, et al. 2009. Precise determination of the diversity of a combinatorial antibody library gives insight into the human immunoglobulin repertoire. Biochemistry. 106(48):20216–21.
   Google Scholar
• Han Y, Li H, Guan Y, and Huang J. 2016. Immune repertoire: a potential biomarker and therapeutic for hepatocellular carcinoma. Cancer Lett. 379(2):206–212.
   PubMedGoogle Scholar
• Howell MC, Green R, McGill AR, Kahlil RM, Dutta R, Mohapatra SS, Mohapatra S. 2021. Activation of intracellular complement in lungs of patients with severe COVID-19 disease decreases T-Cell activity in the lungs. Front Immunol. 12:700705.
   PubMedGoogle Scholar
• Hu X, Zhang J, Wang J, Fu J, Li T, Zheng X, Wang B, Gu S, Jiang P, Fan J, et al. 2019. Landscape of B cell immunity and related immune evasion in human cancers. Nat Genet. 51(3):560–67.
   PubMed Web of Science ®Google Scholar
• Huang L, Shi Y, Gong B, Jiang L, Zhang Z, Liu X, Yang J, He Y, Jiang Z, and Zhong L, et al. 2021. Dynamic blood single-cell immune responses in patients with COVID-19. Signal Transduct Target Ther. 110.
   PubMedGoogle Scholar
• Hwang K-K, Trama AM, Kozink DM, Chen X, Wiehe K, Cooper AJ, Xia S-M, Wang M, Marshall DJ, Whitesides J, et al. 2014. IGHV1-69 B cell chronic lymphocytic leukemia antibodies cross-react with HIV-1 and Hepatitis C Virus antigens as well as intestinal commensal bacteria. PLoS ONE. 9(3):e90725.
   PubMedGoogle Scholar
• Jennewein MF, MacCamy AJ, Akins NR, Feng J, Homad LJ, Hurlburt NK, Seydoux E, Wan Y-H, Stuart AB, Edara VV, et al. 2021. Isolation and characterization of cross-neutralizing coronavirus antibodies from COVID-19+ subjects. Cell Rep. 36(2):109353.
   PubMed Web of Science ®Google Scholar
• Jin X, Zhou W, Luo M, Wang P, Xu Z, Ma K, Cao H, Xu C, Huang Y, Cheng R, et al. 2021. Global characterization of B cell receptor repertoire in COVID-19 patients by single-cell V(D)J sequencing. Brief Bioinform. 22(6). doi:10.1093/bib/bbab192.
   Google Scholar
• Kantor AB, Merrill CE, Herzenberg LA, Hillson JL. 1997. An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J Immunol. 158(3):1175–86.
   PubMed Web of Science ®Google Scholar
• Kostareli E, Sutton L-A, Hadzidimitriou A, Darzentas N, Kouvatsi A, Tsaftaris A, Anagnostopoulos A, Rosenquist R, Stamatopoulos K. 2010. Intraclonal diversification of immunoglobulin light chains in a subset of chronic lymphocytic leukemia alludes to antigen-driven clonal evolution. Leukemia. 24(7):1317–24.
   PubMedGoogle Scholar
• Leng L, Li M, Li W, Mou D, Liu G, Ma J, Zhang S, Li H, Cao R, Zhong W, et al. 2021. Sera proteomic features of active and recovered COVID-19 patients: potential diagnostic and prognostic biomarkers. Signal Transduction Targeted Ther. 6(1):216.
   PubMed Web of Science ®Google Scholar
• Letunic I, Bork P. 2021. Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49(W1):W293–W296.
   PubMed Web of Science ®Google Scholar
• Li F, Luo M, Zhou W, Li J, Jin X, Xu Z, Juan L, Zhang Z, Li Y, Liu R, et al. 2021. Single cell RNA and immune repertoire profiling of COVID-19 patients reveal novel neutralizing antibody. Protein Cell. 12(10):751–55.
   PubMed Web of Science ®Google Scholar
• Lingwood D, McTamney PM, Yassine HM, Whittle JR, Guo X, Boyington JC, Wei CJ, Nabel GJ. 2012. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature. 489(7417):566–570
   PubMed Web of Science ®Google Scholar
• McClain MT, Constantine FJ, Henao R, Liu Y, Tsalik EL, Burke TW, Steinbrink JM, Petzold E, Nicholson BP, Rolfe R, et al. 2020. Dysregulated transcriptional responses to SARS-CoV-2 in the periphery support novel diagnostic approaches. medRxiv: The preprint server for health sciences. 2020.07.20.20155507.
   Google Scholar
• Messmer BT, Albesiano E, Messmer D, Chiorazzi N. 2004. The pattern and distribution of immunoglobulin VH gene mutations in chronic lymphocytic leukemia B cells are consistent with the canonical somatic hypermutation process. Blood. 103(9):3490–95.
   PubMedGoogle Scholar
• Minafò YA, Del Padre M, Cristofoletti C, Caprini E, Perez M, Aranburu A, Colantuono S, Gragnani L, Zignego AL, Pulsoni A, et al. 2020. A stereotyped light chain may shape virus-specific B-cell receptors in HCV-dependent lymphoproliferative disorders. Genes Immun. 21(2):131–35.
   PubMedGoogle Scholar
• Montague Z, Lv H, Otwinowski J, DeWitt WS, Isacchini G, Yip GK, Ng WW, Tsang OTY, Yuan M, Liu H, et al. 2021. Dynamics of B cell repertoires and emergence of cross-reactive responses in patients with different severities of COVID-19. Cell Rep. 35(8):109173.
   PubMed Web of Science ®Google Scholar
• Montecino-Rodriguez E, Dorshkind K. 2006. New perspectives in B-1 B cell development and function. Trends Immunol. 27(9):428–33.
   PubMedGoogle Scholar
• Nielsen SCA, Yang F, Hoh RA, Jackson KJ, Roeltgen K, Lee JY, Rustagi A, Rogers AJ, and Powell AE, et al. 2020. B cell clonal expansion and convergent antibody responses to SARS-CoV-2. Res Square 1 . rs.3.rs–27220.
   Google Scholar
• Niu X, Li S, Li P, Pan W, Wang Q, Feng Y, Mo X, Yan Q, Ye X, Luo J, et al. 2020. Longitudinal analysis of T and B Cell receptor repertoire transcripts reveal dynamic immune response in COVID-19 patients. Front Immunol. 11:582010.
   Google Scholar
• Omayio D, and Mzungu E . 2019. Modification of shannon-wiener diversity index towards quantitative estimation of environmental wellness and biodiversity levels under a non-comparative scenario. J Environ and Earth Sci. 9(9):46–57.
   Google Scholar
• Panovska-Stavridis I, Ridova N, Stojanovska S, Stevanovic M, Stojanoska T, Demiri I, Matevska-Geshkovska N, Vujovic M, Markoska H, Filipce V, et al. 2021. Prevalence of allelic variants and clonality of IGHV1-69 expressing B-cells in patients with different severity of COVID 19 disease. Blood. 138(Suppl 1):994.
   Google Scholar
• Paschold L, Simnica D, Brito RB, Zhang T, Schultheiß C, Dierks C, Binder M. 2022. Subclonal heterogeneity sheds light on the transformation trajectory in IGLV3-21R110 chronic lymphocytic leukemia. Blood Cancer J. 12(3):49.
   PubMedGoogle Scholar
• Pineda S, Sigdel TK, Liberto JM, Vincenti F, Sirota M, Sarwal MM. 2019. Characterizing pre-transplant and post-transplant kidney rejection risk by B cell immune repertoire sequencing. Nat Commun. 10(1):1906.
   PubMedGoogle Scholar
• Rothe C, Schunk M, Sothmann P, Bretzel G, Froeschl G, Wallrauch C, Zimmer T, Thiel V, Janke C, Guggemos W, et al. 2020. Transmission of 2019-nCov Infection from an asymptomatic contact in Germany. N Engl J Med. 382(10):970–71.
   PubMed Web of Science ®Google Scholar
• Schultheiss C, Paschold L, Simnica D, Mohme M, Willscher E, von Wenserski L, Scholz R, Wieters I, Dahlke C, Tolosa E, et al. 2020. Next-generation sequencing of T and B cell receptor repertoires from COVID-19 patients showed signatures associated with severity of disease. Immunity. 53(2):442–55 e4.
   PubMed Web of Science ®Google Scholar
• Schultheiß C, Paschold L, Simnica D, Mohme M, Willscher E, von Wenserski L, Scholz R, Wieters I, Dahlke C, Tolosa E, et al. 2020. Next-Generation sequencing of T and B cell receptor repertoires from COVID-19 patients showed signatures associated with severity of disease. Immunity. 53(2):442–55.e4.
   PubMed Web of Science ®Google Scholar
• Shi Y, Wang G, Cai XP, Deng JW, Zheng L, Zhu HH, Zheng M, Yang B, Chen Z. 2020. An overview of COVID-19. J Zhejiang Univ Sci B. 21(5):343–60.
   PubMed Web of Science ®Google Scholar
• Shugay M, Bagaev DV, Turchaninova MA, Bolotin DA, Britanova OV, Putintseva EV, Pogorelyy MV, Nazarov VI, Zvyagin IV, Kirgizova VI, et al. 2015. VDJtools: Unifying Post-analysis of T Cell Receptor Repertoires. PLoS Comput Biol. 11(11):e1004503.
   PubMed Web of Science ®Google Scholar
• Sindhava V, Bondada S. 2012. Multiple regulatory mechanisms control B-1 B cell activation. Front Immunol. 3:372.
   PubMedGoogle Scholar
• Stamatopoulos K, Belessi C, Hadzidimitriou A, Smilevska T, Kalagiakou E, Hatzi K, Stavroyianni N, thanasiadou A, Tsompanakou A, Papadaki T, et al. 2005. Immunoglobulin light chain repertoire in chronic lymphocytic leukemia. Blood. 106(10):3575–83.
   PubMedGoogle Scholar
• Stamatopoulos B, Smith T, Crompot E, Pieters K, Clifford R, Mraz M, Robbe P, Burns A, Timbs A, Bruce D, et al. 2018. The light chain IgLV3-21 defines a new poor prognostic subgroup in chronic lymphocytic leukemia: results of a multicenter study. Clin Cancer Res. 24(20):5048–57.
   PubMed Web of Science ®Google Scholar
• Tamura K, Stecher G, Kumar S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 38(7):3022–27.
   PubMed Web of Science ®Google Scholar
• Tavakolpour S, Rakhshandehroo T, Wei EX, Rashidian M. 2020. Lymphopenia during the COVID-19 infection: What it shows and what can be learned. Immunol Lett. 225:31–32.
   PubMed Web of Science ®Google Scholar
• Townsend CL, Laffy JMJ, Wu YC, Silva O’Hare J, Martin V, Kipling D, Fraternali F, and Dunn-Walters DK. 2016. Significant differences in physicochemical properties of human immunoglobulin kappa and lambda CDR3 regions. Front Immunol. 7:388 .
   PubMed Web of Science ®Google Scholar
• Tucci FA, Kitanovski S, Johansson P, Klein-Hitpass L, Kahraman A, Dürig J, Hoffmann D, Küppers R. 2018. Biased IGH VDJ gene repertoire and clonal expansions in B cells of chronically hepatitis C virus–infected individuals. Blood. 131(5):546–57.
   PubMedGoogle Scholar
• Vabret N, Britton GJ, Gruber C, Hegde S, Kim J, Kuksin M, Levantovsky R, Malle L, Moreira A, Park MD, et al. 2020. Immunology of COVID-19: current state of the science. Immunity. 52(6):910–41.
   PubMed Web of Science ®Google Scholar
• Voss WN, Hou YJ, Johnson NV, Kim JE, Delidakis G, Horton AP, Bartzoka F, Paresi CJ, Tanno Y, Abbasi SA, Pickens W. 2020. Prevalent, protective, and convergent IgG recognition of SARS-CoV-2 non-RBD spike epitopes in COVID-19 convalescent plasma. bioRxiv. 2020.12.20.423708.
   Google Scholar
• Wang W, Xu Y, Gao R, Lu R, Han K, Wu G, Tan W. 2020. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 323(18):1843–44.
   PubMed Web of Science ®Google Scholar
• Wang Y, Yuan M, Lv H, Peng J, Wilson IA, Wu NC. 2021. A large-scale systematic survey of SARS-CoV-2 antibodies reveals recurring molecular features. bioRxiv. 2021.11.26.470157
   Google Scholar
• Wen W, Su W, Tang H, Le W, Zhang X, Zheng Y, Liu X, Xie L, Li J, Ye J, et al. 2020. Immune cell profiling of COVID-19 patients in the recovery stage by single-cell sequencing. Cell Discovery. 6(1):31.
   PubMed Web of Science ®Google Scholar
• Wong JB, Hewitt SL, Heltemes-Harris LM, Mandal M, Johnson K, Rajewsky K, Koralov SB, Clark MR, Farrar MA, Skok JA. 2019. B-1a cells acquire their unique characteristics by bypassing the pre-BCR selection stage. Nat Commun. 10(1):4768.
   PubMedGoogle Scholar
• Wu Z, McGoogan JM. 2020. Asymptomatic and pre-symptomatic COVID-19 in China. Infect Dis of Poverty. 9(1):72.
   PubMedGoogle Scholar
• Zhang W, Du Y, Su Z, Wang C, Zeng X, Zhang R, Hong X, Nie C, Wu J, Cao H, et al. 2015. Imonitor: a robust pipeline for TCR and BCR repertoire analysis. Genetics. 201(2):459–72.
   PubMed Web of Science ®Google Scholar
• Zhang W, Feng Q, Wang C, Zeng X, Du Y, Lin L, Wu J, Fu L, Yang K, Xu X, et al. 2017. Characterization of the B cell receptor repertoire in the intestinal mucosa and of tumor-infiltrating lymphocytes in colorectal adenoma and carcinoma. J Immun. 198(9):3719–28.
   PubMedGoogle Scholar
• Zhang F, Gan R, Zhen Z, Hu X, Li X, Zhou F, Liu Y, Chen C, Xie S, Zhang B, et al. 2020a. Adaptive immune responses to SARS-CoV-2 infection in severe versus mild individuals. Signal Transduction Targeted Ther. 5(1):156.
   PubMed Web of Science ®Google Scholar
• Zhang J-Y, Wang X-M, Xing X, Xu Z, Zhang C, Song J-W, Fan X, Xia P, Fu J-L, Wang S-Y, et al. 2020b. Single-Cell landscape of immunological responses in patients with COVID-19. Nat Immunol. 21(9):1107–18.
   PubMed Web of Science ®Google Scholar
• Zhao X-N, You Y, Cui X-M, Gao H-X, Wang G-L, Zhang S-B, Yao L, Duan L-J, Zhu K-L, Wang Y-L, et al. 2021. Single-Cell immune profiling reveals distinct immune response in asymptomatic COVID-19 patients. Signal Transduction Targeted Ther. 6(1):342.
   PubMedGoogle Scholar
• Zost SJ, Gilchuk P, Case JB, Binshtein E, Chen RE, Nkolola JP, Schäfer A, Reidy JX, Trivette A, Nargi RS, Sutton RE. 2020. Potently neutralizing and protective human antibodies against SARS-CoV-2. Nature. 584(7821):443–449.
   PubMed Web of Science ®Google Scholar