Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax

Jakub Gruszczyk; Usheer Kanjee; Li Jin Chan; Sébastien Menant; Benoit Malleret; Nicholas T.Y. Lim; Christoph Q. Schmidt; Yee Foong Mok; Kai Min Lin; Richard D. Pearson; Gabriel Rangel; Brian J. Smith; Melissa J. Call; Michael P. Weekes; Michael D.W. Griffin; James M. Murphy; Jonathan Abraham; Kanlaya Sriprawat; Maria J. Menezes; Marcelo U. Ferreira; Bruce Russell; Laurent Renia; Manoj T. Duraisingh; Wai Hong Tham

doi:10.1126/science.aan1078

Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax

Jakub Gruszczyk, Usheer Kanjee, Li Jin Chan, Sébastien Menant, Benoit Malleret, Nicholas T.Y. Lim, Christoph Q. Schmidt, Yee Foong Mok, Kai Min Lin, Richard D. Pearson, Gabriel Rangel, Brian J. Smith, Melissa J. Call, Michael P. Weekes, Michael D.W. Griffin, James M. Murphy, Jonathan Abraham, Kanlaya Sriprawat, Maria J. Menezes, Marcelo U. FerreiraBruce Russell, Laurent Renia, Manoj T. Duraisingh, Wai Hong Tham

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Abstract

Plasmodium vivax shows a strict host tropism for reticulocytes.We identified transferrin receptor 1 (TfR1) as the receptor for P. vivax reticulocyte-binding protein 2b (PvRBP2b).We determined the structure of the N-terminal domain of PvRBP2b involved in red blood cell binding, elucidating the molecular basis for TfR1 recognition.We validated TfR1 as the biological target of PvRBP2b engagement by means of TfR1 expression knockdown analysis. TfR1 mutant cells deficient in PvRBP2b binding were refractory to invasion of P. vivax but not to invasion of P. falciparum. Using Brazilian and Thai clinical isolates, we show that PvRBP2b monoclonal antibodies that inhibit reticulocyte binding also block P. vivax entry into reticulocytes.These data show that TfR1-PvRBP2b invasion pathway is critical for the recognition of reticulocytes during P. vivax invasion.

Original language	English
Pages (from-to)	48-55
Number of pages	8
Journal	Science
Volume	359
Issue number	6371
DOIs	https://doi.org/10.1126/science.aan1078
Publication status	Published - 5 Jan 2018
Externally published	Yes

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Gruszczyk, J., Kanjee, U., Chan, L. J., Menant, S., Malleret, B., Lim, N. T. Y., Schmidt, C. Q., Mok, Y. F., Lin, K. M., Pearson, R. D., Rangel, G., Smith, B. J., Call, M. J., Weekes, M. P., Griffin, M. D. W., Murphy, J. M., Abraham, J., Sriprawat, K., Menezes, M. J., ... Tham, W. H. (2018). Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax. Science, 359(6371), 48-55. https://doi.org/10.1126/science.aan1078

@article{9c8b1a6eedec4c47b3aa85a073aba126,

title = "Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax",

abstract = "Plasmodium vivax shows a strict host tropism for reticulocytes.We identified transferrin receptor 1 (TfR1) as the receptor for P. vivax reticulocyte-binding protein 2b (PvRBP2b).We determined the structure of the N-terminal domain of PvRBP2b involved in red blood cell binding, elucidating the molecular basis for TfR1 recognition.We validated TfR1 as the biological target of PvRBP2b engagement by means of TfR1 expression knockdown analysis. TfR1 mutant cells deficient in PvRBP2b binding were refractory to invasion of P. vivax but not to invasion of P. falciparum. Using Brazilian and Thai clinical isolates, we show that PvRBP2b monoclonal antibodies that inhibit reticulocyte binding also block P. vivax entry into reticulocytes.These data show that TfR1-PvRBP2b invasion pathway is critical for the recognition of reticulocytes during P. vivax invasion.",

author = "Jakub Gruszczyk and Usheer Kanjee and Chan, {Li Jin} and S{\'e}bastien Menant and Benoit Malleret and Lim, {Nicholas T.Y.} and Schmidt, {Christoph Q.} and Mok, {Yee Foong} and Lin, {Kai Min} and Pearson, {Richard D.} and Gabriel Rangel and Smith, {Brian J.} and Call, {Melissa J.} and Weekes, {Michael P.} and Griffin, {Michael D.W.} and Murphy, {James M.} and Jonathan Abraham and Kanlaya Sriprawat and Menezes, {Maria J.} and Ferreira, {Marcelo U.} and Bruce Russell and Laurent Renia and Duraisingh, {Manoj T.} and Tham, {Wai Hong}",

note = "Funding Information: We thank J. Newman from the Commonwealth Scientific and Industrial Research Organization Collaborative Crystallization Centre for assistance with setting up the crystallization screens, the Walter and Eliza Hall Institute{\textquoteright}s Monoclonal Antibody Facility for production of antibodies, J. Williamson for assistance with mass spectrometry, and MX and SAXS beamline staff at the Australian Synchrotron for their assistance during data collection. We thank F. Nosten, the staff and patients attending the Mae Sot Malaria Clinic in Thailand, and clinics associated with the Shoklo Malaria Research Unit (SMRU), Tak Province, Thailand. We also thank Y. Colin and O. S. Bertrand (INSERM/University Paris 7) for the generous gift of the antibodies to DARC. W.-H.T. is a Howard Hughes Medical Institute–Wellcome Trust International Research Scholar (208693/Z/17/Z). This work was supported in part by the Australian Research Council Future Fellowships to W.-H.T. and M.D.W.G., a Speedy Innovation Grant to W.-H.T., and a National Health and Medical Research Council fellowship (1105754) to J.M.M. U.K. was supported by a Canadian Institutes of Health Research Postdoctoral Fellowship. R.D.P. is funded by Wellcome Trust 090770. M.P.W. was supported by a Wellcome Trust Senior Clinical Research Fellowship (108070/Z/15/ Z). This study received funding from Singapore National Medical Research Council (NMRC) (NMRC/CBRG/0047/2013) and the Agency for Science, Technology and Research (A*STAR, Singapore). SMRU is sponsored by The Wellcome Trust of Great Britain as part of the Oxford Tropical Medicine Research Programme of Wellcome Trust–Mahidol University. Work in the M.T.D. laboratory was supported by National Institutes of Health grant 1R01HL139337. We also acknowledge the support of the B.R. laboratory from the Marsden Fund 17-UOO-241.The authors acknowledge the Victorian State Government Operational Infrastructure Support and Australian Government National Health and Medical Research Council Independent Research Institute Infrastructure Support Scheme. All data and code to understand and assess the conclusions of this research are available in the main text, supplementary materials, and via the following repositories: The atomic coordinates and structure factors for PvRBP2b have been deposited in PDB with accession number 5W53. Genotypes were derived from sequence data generated at the Wellcome Trust Sanger Institute (Wellcome Trust 206194 and 098051).",

year = "2018",

month = jan,

day = "5",

doi = "10.1126/science.aan1078",

language = "English",

volume = "359",

pages = "48--55",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science (AAAS)",

number = "6371",

}

Gruszczyk, J, Kanjee, U, Chan, LJ, Menant, S, Malleret, B, Lim, NTY, Schmidt, CQ, Mok, YF, Lin, KM, Pearson, RD, Rangel, G, Smith, BJ, Call, MJ, Weekes, MP, Griffin, MDW, Murphy, JM, Abraham, J, Sriprawat, K, Menezes, MJ, Ferreira, MU, Russell, B, Renia, L, Duraisingh, MT & Tham, WH 2018, 'Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax', Science, vol. 359, no. 6371, pp. 48-55. https://doi.org/10.1126/science.aan1078

TY - JOUR

T1 - Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax

AU - Gruszczyk, Jakub

AU - Kanjee, Usheer

AU - Chan, Li Jin

AU - Menant, Sébastien

AU - Malleret, Benoit

AU - Lim, Nicholas T.Y.

AU - Schmidt, Christoph Q.

AU - Mok, Yee Foong

AU - Lin, Kai Min

AU - Pearson, Richard D.

AU - Rangel, Gabriel

AU - Smith, Brian J.

AU - Call, Melissa J.

AU - Weekes, Michael P.

AU - Griffin, Michael D.W.

AU - Murphy, James M.

AU - Abraham, Jonathan

AU - Sriprawat, Kanlaya

AU - Menezes, Maria J.

AU - Ferreira, Marcelo U.

AU - Russell, Bruce

AU - Renia, Laurent

AU - Duraisingh, Manoj T.

AU - Tham, Wai Hong

N1 - Funding Information: We thank J. Newman from the Commonwealth Scientific and Industrial Research Organization Collaborative Crystallization Centre for assistance with setting up the crystallization screens, the Walter and Eliza Hall Institute’s Monoclonal Antibody Facility for production of antibodies, J. Williamson for assistance with mass spectrometry, and MX and SAXS beamline staff at the Australian Synchrotron for their assistance during data collection. We thank F. Nosten, the staff and patients attending the Mae Sot Malaria Clinic in Thailand, and clinics associated with the Shoklo Malaria Research Unit (SMRU), Tak Province, Thailand. We also thank Y. Colin and O. S. Bertrand (INSERM/University Paris 7) for the generous gift of the antibodies to DARC. W.-H.T. is a Howard Hughes Medical Institute–Wellcome Trust International Research Scholar (208693/Z/17/Z). This work was supported in part by the Australian Research Council Future Fellowships to W.-H.T. and M.D.W.G., a Speedy Innovation Grant to W.-H.T., and a National Health and Medical Research Council fellowship (1105754) to J.M.M. U.K. was supported by a Canadian Institutes of Health Research Postdoctoral Fellowship. R.D.P. is funded by Wellcome Trust 090770. M.P.W. was supported by a Wellcome Trust Senior Clinical Research Fellowship (108070/Z/15/ Z). This study received funding from Singapore National Medical Research Council (NMRC) (NMRC/CBRG/0047/2013) and the Agency for Science, Technology and Research (A*STAR, Singapore). SMRU is sponsored by The Wellcome Trust of Great Britain as part of the Oxford Tropical Medicine Research Programme of Wellcome Trust–Mahidol University. Work in the M.T.D. laboratory was supported by National Institutes of Health grant 1R01HL139337. We also acknowledge the support of the B.R. laboratory from the Marsden Fund 17-UOO-241.The authors acknowledge the Victorian State Government Operational Infrastructure Support and Australian Government National Health and Medical Research Council Independent Research Institute Infrastructure Support Scheme. All data and code to understand and assess the conclusions of this research are available in the main text, supplementary materials, and via the following repositories: The atomic coordinates and structure factors for PvRBP2b have been deposited in PDB with accession number 5W53. Genotypes were derived from sequence data generated at the Wellcome Trust Sanger Institute (Wellcome Trust 206194 and 098051).

PY - 2018/1/5

Y1 - 2018/1/5

N2 - Plasmodium vivax shows a strict host tropism for reticulocytes.We identified transferrin receptor 1 (TfR1) as the receptor for P. vivax reticulocyte-binding protein 2b (PvRBP2b).We determined the structure of the N-terminal domain of PvRBP2b involved in red blood cell binding, elucidating the molecular basis for TfR1 recognition.We validated TfR1 as the biological target of PvRBP2b engagement by means of TfR1 expression knockdown analysis. TfR1 mutant cells deficient in PvRBP2b binding were refractory to invasion of P. vivax but not to invasion of P. falciparum. Using Brazilian and Thai clinical isolates, we show that PvRBP2b monoclonal antibodies that inhibit reticulocyte binding also block P. vivax entry into reticulocytes.These data show that TfR1-PvRBP2b invasion pathway is critical for the recognition of reticulocytes during P. vivax invasion.

AB - Plasmodium vivax shows a strict host tropism for reticulocytes.We identified transferrin receptor 1 (TfR1) as the receptor for P. vivax reticulocyte-binding protein 2b (PvRBP2b).We determined the structure of the N-terminal domain of PvRBP2b involved in red blood cell binding, elucidating the molecular basis for TfR1 recognition.We validated TfR1 as the biological target of PvRBP2b engagement by means of TfR1 expression knockdown analysis. TfR1 mutant cells deficient in PvRBP2b binding were refractory to invasion of P. vivax but not to invasion of P. falciparum. Using Brazilian and Thai clinical isolates, we show that PvRBP2b monoclonal antibodies that inhibit reticulocyte binding also block P. vivax entry into reticulocytes.These data show that TfR1-PvRBP2b invasion pathway is critical for the recognition of reticulocytes during P. vivax invasion.

UR - http://www.scopus.com/inward/record.url?scp=85040101798&partnerID=8YFLogxK

U2 - 10.1126/science.aan1078

DO - 10.1126/science.aan1078

M3 - Article

C2 - 29302006

AN - SCOPUS:85040101798

SN - 0036-8075

VL - 359

SP - 48

EP - 55

JO - Science

JF - Science

IS - 6371

ER -

Transferrin receptor 1 is a reticulocyte-specific receptor for Plasmodium vivax

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