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RAIN: machine learning-based identification for HIV-1 bNAbs

Author

Listed:
  • Mathilde Foglierini

    (Lausanne University Hospital and University of Lausanne
    Centre for Human Immunology
    Lausanne University Hospital and University of Lausanne)

  • Pauline Nortier

    (Lausanne University Hospital and University of Lausanne
    Centre for Human Immunology)

  • Rachel Schelling

    (Lausanne University Hospital and University of Lausanne
    Centre for Human Immunology)

  • Rahel R. Winiger

    (Lausanne University Hospital and University of Lausanne
    Centre for Human Immunology)

  • Philippe Jacquet

    (University of Lausanne)

  • Sijy O’Dell

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Davide Demurtas

    (CIME, Ecole Polytechnique Fédérale de Lausanne)

  • Maxmillian Mpina

    (Ifakara Health Institute)

  • Omar Lweno

    (Ifakara Health Institute)

  • Yannick D. Muller

    (Lausanne University Hospital and University of Lausanne
    Centre for Human Immunology)

  • Constantinos Petrovas

    (Lausanne University Hospital)

  • Claudia Daubenberger

    (Clinical Immunology Unit, Swiss Tropical and Public Health Institute
    University of Basel)

  • Matthieu Perreau

    (Lausanne University Hospital and University of Lausanne)

  • Nicole A. Doria-Rose

    (National Institute of Allergy and Infectious Diseases, National Institutes of Health)

  • Raphael Gottardo

    (Lausanne University Hospital and University of Lausanne)

  • Laurent Perez

    (Lausanne University Hospital and University of Lausanne
    Centre for Human Immunology)

Abstract

Broadly neutralizing antibodies (bNAbs) are promising candidates for the treatment and prevention of HIV-1 infections. Despite their critical importance, automatic detection of HIV-1 bNAbs from immune repertoires is still lacking. Here, we develop a straightforward computational method for the Rapid Automatic Identification of bNAbs (RAIN) based on machine learning methods. In contrast to other approaches, which use one-hot encoding amino acid sequences or structural alignment for prediction, RAIN uses a combination of selected sequence-based features for the accurate prediction of HIV-1 bNAbs. We demonstrate the performance of our approach on non-biased, experimentally obtained and sequenced BCR repertoires from HIV-1 immune donors. RAIN processing leads to the successful identification of distinct HIV-1 bNAbs targeting the CD4-binding site of the envelope glycoprotein. In addition, we validate the identified bNAbs using an in vitro neutralization assay and we solve the structure of one of them in complex with the soluble native-like heterotrimeric envelope glycoprotein by single-particle cryo-electron microscopy (cryo-EM). Overall, we propose a method to facilitate and accelerate HIV-1 bNAbs discovery from non-selected immune repertoires.

Suggested Citation

  • Mathilde Foglierini & Pauline Nortier & Rachel Schelling & Rahel R. Winiger & Philippe Jacquet & Sijy O’Dell & Davide Demurtas & Maxmillian Mpina & Omar Lweno & Yannick D. Muller & Constantinos Petrov, 2024. "RAIN: machine learning-based identification for HIV-1 bNAbs," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49676-1
    DOI: 10.1038/s41467-024-49676-1
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    1. Masashi Shingai & Yoshiaki Nishimura & Florian Klein & Hugo Mouquet & Olivia K. Donau & Ronald Plishka & Alicia Buckler-White & Michael Seaman & Michael Piatak & Jeffrey D. Lifson & Dimiter Dimitrov &, 2013. "Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia," Nature, Nature, vol. 503(7475), pages 277-280, November.
    2. Wenwei Li & Zhuan Qin & Elizabeth Nand & Michael W. Grunst & Jonathan R. Grover & Julian W. Bess & Jeffrey D. Lifson & Michael B. Zwick & Hemant D. Tagare & Pradeep D. Uchil & Walther Mothes, 2023. "HIV-1 Env trimers asymmetrically engage CD4 receptors in membranes," Nature, Nature, vol. 623(7989), pages 1026-1033, November.
    3. Pilar Mendoza & Henning Gruell & Lilian Nogueira & Joy A. Pai & Allison L. Butler & Katrina Millard & Clara Lehmann & Isabelle Suárez & Thiago Y. Oliveira & Julio C. C. Lorenzi & Yehuda Z. Cohen & Chr, 2018. "Combination therapy with anti-HIV-1 antibodies maintains viral suppression," Nature, Nature, vol. 561(7724), pages 479-484, September.
    4. Christian Gaebler & Lilian Nogueira & Elina Stoffel & Thiago Y. Oliveira & Gaëlle Breton & Katrina G. Millard & Martina Turroja & Allison Butler & Victor Ramos & Michael S. Seaman & Jacqueline D. Ree, 2022. "Prolonged viral suppression with anti-HIV-1 antibody therapy," Nature, Nature, vol. 606(7913), pages 368-374, June.
    5. Michael C. Sneller & Jana Blazkova & J. Shawn Justement & Victoria Shi & Brooke D. Kennedy & Kathleen Gittens & Jekaterina Tolstenko & Genevieve McCormack & Emily J. Whitehead & Rachel F. Schneck & Mi, 2022. "Combination anti-HIV antibodies provide sustained virological suppression," Nature, Nature, vol. 606(7913), pages 375-381, June.
    6. Hua-Xin Liao & Rebecca Lynch & Tongqing Zhou & Feng Gao & S. Munir Alam & Scott D. Boyd & Andrew Z. Fire & Krishna M. Roskin & Chaim A. Schramm & Zhenhai Zhang & Jiang Zhu & Lawrence Shapiro & James C, 2013. "Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus," Nature, Nature, vol. 496(7446), pages 469-476, April.
    7. Rajeev Gautam & Yoshiaki Nishimura & Amarendra Pegu & Martha C. Nason & Florian Klein & Anna Gazumyan & Jovana Golijanin & Alicia Buckler-White & Reza Sadjadpour & Keyun Wang & Zachary Mankoff & Steph, 2016. "A single injection of anti-HIV-1 antibodies protects against repeated SHIV challenges," Nature, Nature, vol. 533(7601), pages 105-109, May.
    8. Peter D. Kwong & Michael L. Doyle & David J. Casper & Claudia Cicala & Stephanie A. Leavitt & Shahzad Majeed & Tavis D. Steenbeke & Miro Venturi & Irwin Chaiken & Michael Fung & Hermann Katinger & Pau, 2002. "HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites," Nature, Nature, vol. 420(6916), pages 678-682, December.
    9. Marie Pancera & Tongqing Zhou & Aliaksandr Druz & Ivelin S. Georgiev & Cinque Soto & Jason Gorman & Jinghe Huang & Priyamvada Acharya & Gwo-Yu Chuang & Gilad Ofek & Guillaume B. E. Stewart-Jones & Jon, 2014. "Structure and immune recognition of trimeric pre-fusion HIV-1 Env," Nature, Nature, vol. 514(7523), pages 455-461, October.
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