Treg-Cell-Derived IL-35-Coated Extracellular Vesicles Promote Infectious Tolerance

Jeremy A. Sullivan; Yusuke Tomita; Ewa Jankowska-Gan; Diego A. Lema; Matt P. Arvedson; Ashita Nair; William Bracamonte-Baran; Ying Zhou; Kristy K. Meyer; Weixiong Zhong; Deepali V. Sawant; Andrea L. Szymczak-Workman; Qianxia Zhang; Creg J. Workman; Seungpyo Hong; Dario A.A. Vignali; William J. Burlingham

doi:10.1016/j.celrep.2019.12.081

Treg-Cell-Derived IL-35-Coated Extracellular Vesicles Promote Infectious Tolerance

Jeremy A. Sullivan, Yusuke Tomita, Ewa Jankowska-Gan, Diego A. Lema, Matt P. Arvedson, Ashita Nair, William Bracamonte-Baran, Ying Zhou, Kristy K. Meyer, Weixiong Zhong, Deepali V. Sawant, Andrea L. Szymczak-Workman, Qianxia Zhang, Creg J. Workman, Seungpyo Hong, Dario A.A. Vignali, William J. Burlingham

Department of Pharmacy

Research output: Contribution to journal › Article › peer-review

59 Citations (Scopus)

Abstract

Sullivan et al. show that while many factors and cytokines contribute to primary immunosuppression, EV-associated IL-35 uniquely promotes “infectious” tolerance not only by inducing IL-35 production in non-Treg cells but also by causing an immunosuppressive phenotype in EV-acquiring T and B cells, leading to secondary suppression of immune responses.

Original language	English
Pages (from-to)	1039-1051.e5
Journal	Cell Reports
Volume	30
Issue number	4
DOIs	https://doi.org/10.1016/j.celrep.2019.12.081
Publication status	Published - 2020 Jan 28

Bibliographical note

Funding Information:
We wish to thank Dagna Sheerar and the personnel of the UW Carbone Cancer Center Flow Laboratory for technical support on flow cytometry and Image Stream experiments. We also acknowledge the support of Dr. Anita Chong and Dr. Marisa Alegre and their labs at the University of Chicago for providing splenocytes from BALB/c × C57BL/6 [Tg for mOVA-2W1S] mice for tolerization studies and Scott Burlingham for discussion and suggestions. This project was supported by the NIH (grant R01-AI119140-03 to W.J.B., R03-144-AAH5568 to J.A.S. and grants R01 CA203689 and P30 CA047904 to D.A.A.V.) and University of Wisconsin Carbone Cancer Center (support grant P30 CA014520 ).

Funding Information:
We wish to thank Dagna Sheerar and the personnel of the UW Carbone Cancer Center Flow Laboratory for technical support on flow cytometry and Image Stream experiments. We also acknowledge the support of Dr. Anita Chong and Dr. Marisa Alegre and their labs at the University of Chicago for providing splenocytes from BALB/c ? C57BL/6 [Tg for mOVA-2W1S] mice for tolerization studies and Scott Burlingham for discussion and suggestions. This project was supported by the NIH (grant R01-AI119140-03 to W.J.B. R03-144-AAH5568 to J.A.S. and grants R01 CA203689 and P30 CA047904 to D.A.A.V.) and University of Wisconsin Carbone Cancer Center (support grant P30 CA014520). Conceptualization, J.A.S. D.A.A.V. W.J.B. and E.J.-G.; Methodology, J.A.S. Y.T. D.A.L. E.J.-G. W.B.-B. W.Z. D.W.S. A.L.S.-W. Q.Z. K.K.M. C.J.W. and S.H.; Investigation, J.A.S. W.J.B. E.J.-G. A.N. D.A.L. M.P.A. and Y.T.; Writing ? Original Draft, J.A.S. W.J.B. E.J.G. Y.T. and D.A.A.V.; Writing ? Review & Editing, J.A.S. E.J.G. D.A.A.V. C.J.W. M.P.A. and W.J.B.; Funding Acquisition, W.J.B. and D.A.A.V.; Resources, D.A.A.V. W.J.B. and S.H.; Supervision, J.A.S. D.A.A.V. S.H. and W.J.B. The authors declare no competing interests.

Publisher Copyright:
© 2019 The Author(s)

All Science Journal Classification (ASJC) codes

Biochemistry, Genetics and Molecular Biology(all)

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10.1016/j.celrep.2019.12.081

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Sullivan, J. A., Tomita, Y., Jankowska-Gan, E., Lema, D. A., Arvedson, M. P., Nair, A., Bracamonte-Baran, W., Zhou, Y., Meyer, K. K., Zhong, W., Sawant, D. V., Szymczak-Workman, A. L., Zhang, Q., Workman, C. J., Hong, S., Vignali, D. A. A., & Burlingham, W. J. (2020). Treg-Cell-Derived IL-35-Coated Extracellular Vesicles Promote Infectious Tolerance. Cell Reports, 30(4), 1039-1051.e5. https://doi.org/10.1016/j.celrep.2019.12.081

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abstract = "Sullivan et al. show that while many factors and cytokines contribute to primary immunosuppression, EV-associated IL-35 uniquely promotes “infectious” tolerance not only by inducing IL-35 production in non-Treg cells but also by causing an immunosuppressive phenotype in EV-acquiring T and B cells, leading to secondary suppression of immune responses.",

author = "Sullivan, {Jeremy A.} and Yusuke Tomita and Ewa Jankowska-Gan and Lema, {Diego A.} and Arvedson, {Matt P.} and Ashita Nair and William Bracamonte-Baran and Ying Zhou and Meyer, {Kristy K.} and Weixiong Zhong and Sawant, {Deepali V.} and Szymczak-Workman, {Andrea L.} and Qianxia Zhang and Workman, {Creg J.} and Seungpyo Hong and Vignali, {Dario A.A.} and Burlingham, {William J.}",

note = "Funding Information: We wish to thank Dagna Sheerar and the personnel of the UW Carbone Cancer Center Flow Laboratory for technical support on flow cytometry and Image Stream experiments. We also acknowledge the support of Dr. Anita Chong and Dr. Marisa Alegre and their labs at the University of Chicago for providing splenocytes from BALB/c × C57BL/6 [Tg for mOVA-2W1S] mice for tolerization studies and Scott Burlingham for discussion and suggestions. This project was supported by the NIH (grant R01-AI119140-03 to W.J.B., R03-144-AAH5568 to J.A.S. and grants R01 CA203689 and P30 CA047904 to D.A.A.V.) and University of Wisconsin Carbone Cancer Center (support grant P30 CA014520 ). Funding Information: We wish to thank Dagna Sheerar and the personnel of the UW Carbone Cancer Center Flow Laboratory for technical support on flow cytometry and Image Stream experiments. We also acknowledge the support of Dr. Anita Chong and Dr. Marisa Alegre and their labs at the University of Chicago for providing splenocytes from BALB/c ? C57BL/6 [Tg for mOVA-2W1S] mice for tolerization studies and Scott Burlingham for discussion and suggestions. This project was supported by the NIH (grant R01-AI119140-03 to W.J.B. R03-144-AAH5568 to J.A.S. and grants R01 CA203689 and P30 CA047904 to D.A.A.V.) and University of Wisconsin Carbone Cancer Center (support grant P30 CA014520). Conceptualization, J.A.S. D.A.A.V. W.J.B. and E.J.-G.; Methodology, J.A.S. Y.T. D.A.L. E.J.-G. W.B.-B. W.Z. D.W.S. A.L.S.-W. Q.Z. K.K.M. C.J.W. and S.H.; Investigation, J.A.S. W.J.B. E.J.-G. A.N. D.A.L. M.P.A. and Y.T.; Writing ? Original Draft, J.A.S. W.J.B. E.J.G. Y.T. and D.A.A.V.; Writing ? Review & Editing, J.A.S. E.J.G. D.A.A.V. C.J.W. M.P.A. and W.J.B.; Funding Acquisition, W.J.B. and D.A.A.V.; Resources, D.A.A.V. W.J.B. and S.H.; Supervision, J.A.S. D.A.A.V. S.H. and W.J.B. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2019 The Author(s)",

year = "2020",

month = jan,

day = "28",

doi = "10.1016/j.celrep.2019.12.081",

language = "English",

volume = "30",

pages = "1039--1051.e5",

journal = "Cell Reports",

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Sullivan, JA, Tomita, Y, Jankowska-Gan, E, Lema, DA, Arvedson, MP, Nair, A, Bracamonte-Baran, W, Zhou, Y, Meyer, KK, Zhong, W, Sawant, DV, Szymczak-Workman, AL, Zhang, Q, Workman, CJ, Hong, S, Vignali, DAA & Burlingham, WJ 2020, 'Treg-Cell-Derived IL-35-Coated Extracellular Vesicles Promote Infectious Tolerance', Cell Reports, vol. 30, no. 4, pp. 1039-1051.e5. https://doi.org/10.1016/j.celrep.2019.12.081

TY - JOUR

T1 - Treg-Cell-Derived IL-35-Coated Extracellular Vesicles Promote Infectious Tolerance

AU - Sullivan, Jeremy A.

AU - Tomita, Yusuke

AU - Jankowska-Gan, Ewa

AU - Lema, Diego A.

AU - Arvedson, Matt P.

AU - Nair, Ashita

AU - Bracamonte-Baran, William

AU - Zhou, Ying

AU - Meyer, Kristy K.

AU - Zhong, Weixiong

AU - Sawant, Deepali V.

AU - Szymczak-Workman, Andrea L.

AU - Zhang, Qianxia

AU - Workman, Creg J.

AU - Hong, Seungpyo

AU - Vignali, Dario A.A.

AU - Burlingham, William J.

N1 - Funding Information: We wish to thank Dagna Sheerar and the personnel of the UW Carbone Cancer Center Flow Laboratory for technical support on flow cytometry and Image Stream experiments. We also acknowledge the support of Dr. Anita Chong and Dr. Marisa Alegre and their labs at the University of Chicago for providing splenocytes from BALB/c × C57BL/6 [Tg for mOVA-2W1S] mice for tolerization studies and Scott Burlingham for discussion and suggestions. This project was supported by the NIH (grant R01-AI119140-03 to W.J.B., R03-144-AAH5568 to J.A.S. and grants R01 CA203689 and P30 CA047904 to D.A.A.V.) and University of Wisconsin Carbone Cancer Center (support grant P30 CA014520 ). Funding Information: We wish to thank Dagna Sheerar and the personnel of the UW Carbone Cancer Center Flow Laboratory for technical support on flow cytometry and Image Stream experiments. We also acknowledge the support of Dr. Anita Chong and Dr. Marisa Alegre and their labs at the University of Chicago for providing splenocytes from BALB/c ? C57BL/6 [Tg for mOVA-2W1S] mice for tolerization studies and Scott Burlingham for discussion and suggestions. This project was supported by the NIH (grant R01-AI119140-03 to W.J.B. R03-144-AAH5568 to J.A.S. and grants R01 CA203689 and P30 CA047904 to D.A.A.V.) and University of Wisconsin Carbone Cancer Center (support grant P30 CA014520). Conceptualization, J.A.S. D.A.A.V. W.J.B. and E.J.-G.; Methodology, J.A.S. Y.T. D.A.L. E.J.-G. W.B.-B. W.Z. D.W.S. A.L.S.-W. Q.Z. K.K.M. C.J.W. and S.H.; Investigation, J.A.S. W.J.B. E.J.-G. A.N. D.A.L. M.P.A. and Y.T.; Writing ? Original Draft, J.A.S. W.J.B. E.J.G. Y.T. and D.A.A.V.; Writing ? Review & Editing, J.A.S. E.J.G. D.A.A.V. C.J.W. M.P.A. and W.J.B.; Funding Acquisition, W.J.B. and D.A.A.V.; Resources, D.A.A.V. W.J.B. and S.H.; Supervision, J.A.S. D.A.A.V. S.H. and W.J.B. The authors declare no competing interests. Publisher Copyright: © 2019 The Author(s)

PY - 2020/1/28

Y1 - 2020/1/28

N2 - Sullivan et al. show that while many factors and cytokines contribute to primary immunosuppression, EV-associated IL-35 uniquely promotes “infectious” tolerance not only by inducing IL-35 production in non-Treg cells but also by causing an immunosuppressive phenotype in EV-acquiring T and B cells, leading to secondary suppression of immune responses.

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Treg-Cell-Derived IL-35-Coated Extracellular Vesicles Promote Infectious Tolerance

Abstract

Bibliographical note

All Science Journal Classification (ASJC) codes

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