Faculty Appointments
Assistant Professor of Medicine
Assistant Professor of Pathology, Microbiology and Immunology
Education
Ph.D., Microbiology and Immunology, Vanderbilt University, Nashville, TennesseeB.S., Microbiology and Cell Sciences, University of Florida, Gainesville, Florida
Office Address
MCN T3207F
1161 21st Ave. S
Nashville, TN 37232
1161 21st Ave. S
Nashville, TN 37232
Research Description
Autoantibodies serve as predictive and diagnostic biomarkers in many autoimmune diseases, including type 1 diabetes and myositis. Despite the clear role of autoreactive B lymphocytes in these and other autoimmune diseases, the pathways that drive their expansion and differentiation into antibody-secreting cells are not fully understood. My laboratory is harnessing the most cutting-edge, single-cell approaches available to understand how autoantigen-specific B lymphocytes breach immune tolerance to expand. This information is necessary to support the development of new, highly-selective immunomodulatory therapies to prevent further autoimmune destruction.
Research Keywords
B cell, T cell, autoimmunity, antibody, type 1 diabetes, myositis, Sjogren's syndrome, immune checkpoint inhibitor-induced autoimmunity
Publications
Wilfong EM, Vowell KN, Bunn KE, Rizzi E, Annapureddy N, Dudenhofer RB, Barnado A, Bonami RH, Johnson JE, Crofford LJ, Kendall PL. Wilfong, E.M., Vowell, K.N., Bunn, KE., Rizzi, E., Annapureddy, N., Dudenhofer, R.B., Barnado, A., Bonami, R.H., Johnson, J.E., Crofford, L.J., and Kendall, P.L. CD19+CD21lo/neg cells are increased in SSc-ILD. Clinical and Experimental Medicine, 2021, In press. Clin Exp Med [print-electronic]. 2021 Aug 8/10/2021; PMID: 34374937, PII: 10.1007/s10238-021-00745-5, DOI: 10.1007/s10238-021-00745-5, ISSN: 1591-9528.
Kramer KJ, Wilfong EM, Voss K, Barone SM, Shiakolas AR, Raju N, Roe CE, Suryadevara N, Walker L, Wall SC, Paulo A, Schaefer S, Dahunsi D, Westlake CS, Crowe JE, Carnahan RH, Rathmell JC, Bonami RH, Georgiev IS, Irish JM. Single-Cell Profiling of the Antigen-Specific Response to BNT162b2 SARS-CoV-2 RNA Vaccine. BioRxiv. 2021 Jul 7/28/2021; PMID: 34341788, PMCID: PMC8328055, DOI: 10.1101/2021.07.28.453981.
Young-Glazer J, Cisneros A, Wilfong EM, Smith SA, Crofford LJ, Bonami RH. Jo-1 autoantigen-specific B cells are skewed towards distinct functional B cell subsets in anti-synthetase syndrome patients. Arthritis Res Ther. 2021 Jan 1/19/2021; 23(1): 33. PMID: 33468230, PMCID: PMC7814460, PII: 10.1186/s13075-020-02412-8, DOI: 10.1186/s13075-020-02412-8, ISSN: 1478-6362.
Felton JL, Conway H, Bonami RH. B Quiet: Autoantigen-Specific Strategies to Silence Raucous B Lymphocytes and Halt Cross-Talk with T Cells in Type 1 Diabetes. Biomedicines. 2021 Jan 1/6/2021; 9(1): PMID: 33418839, PMCID: PMC7824835, PII: biomedicines9010042, DOI: 10.3390/biomedicines9010042, ISSN: 2227-9059.
Joosse BA, Jackson JH, Cisneros A, Santhin AB, Smith SA, Moore DJ, Crofford LJ, Wilfong EM, Bonami RH. High-Throughput Detection of Autoantigen-Specific B Cells Among Distinct Functional Subsets in Autoimmune Donors. Front Immunol. 2021; 12: 685718. PMID: 34234784, PMCID: PMC8256427, DOI: 10.3389/fimmu.2021.685718, ISSN: 1664-3224.
Bonami RH, Nyhoff LE, McNitt DH, Hulbert C, Felton JL, Kendall PL, Thomas JW. T-B Lymphocyte Interactions Promote Type 1 Diabetes Independently of SLAM-Associated Protein. J Immunol [print-electronic]. 2020 Dec 12/15/2020; 205(12): 3263-76. PMID: 33199538, PMCID: PMC7725913, PII: jimmunol.1900464, DOI: 10.4049/jimmunol.1900464, ISSN: 1550-6606.
Jackson MA, Bedingfield SK, Yu F, Stokan ME, Miles RE, Curvino EJ, Hoogenboezem EN, Bonami RH, Patel SS, Kendall PL, Giorgio TD, Duvall CL. Dual carrier-cargo hydrophobization and charge ratio optimization improve the systemic circulation and safety of zwitterionic nano-polyplexes. Biomaterials [print-electronic]. 2019 Feb; 192: 245-59. PMID: 30458360, PMCID: PMC6534819, PII: S0142-9612(18)30787-7, DOI: 10.1016/j.biomaterials.2018.11.010, ISSN: 1878-5905.
Wilson CS, Chhabra P, Marshall AF, Morr CV, Stocks BT, Hoopes EM, Bonami RH, Poffenberger G, Brayman KL, Moore DJ. Healthy Donor Polyclonal IgMs Diminish B-Lymphocyte Autoreactivity, Enhance Regulatory T-Cell Generation, and Reverse Type 1 Diabetes in NOD Mice. Diabetes [print-electronic]. 2018 Nov; 67(11): 2349-60. PMID: 30131391, PMCID: PMC6198348, PII: db18-0456, DOI: 10.2337/db18-0456, ISSN: 1939-327X.
Felton JL, Maseda D, Bonami RH, Hulbert C, Thomas JW. Anti-Insulin B Cells Are Poised for Antigen Presentation in Type 1 Diabetes. J. Immunol [print-electronic]. 2018 Aug 8/1/2018; 201(3): 861-73. PMID: 29950508, PII: jimmunol.1701717, DOI: 10.4049/jimmunol.1701717, ISSN: 1550-6606.
Nyhoff LE, Clark ES, Barron BL, Bonami RH, Khan WN, Kendall PL. Bruton's Tyrosine Kinase Is Not Essential for B Cell Survival beyond Early Developmental Stages. J. Immunol [print-electronic]. 2018 Apr 4/1/2018; 200(7): 2352-61. PMID: 29483358, PMCID: PMC6177684, PII: jimmunol.1701489, DOI: 10.4049/jimmunol.1701489, ISSN: 1550-6606.
Nyhoff LE, Barron BL, Johnson EM, Bonami RH, Maseda D, Fensterheim BA, Han W, Blackwell TS, Crofford LJ, Kendall PL. Bruton's Tyrosine Kinase Deficiency Inhibits Autoimmune Arthritis in Mice but Fails to Block Immune Complex-Mediated Inflammatory Arthritis. Arthritis & rheumatology (Hoboken, N.J.). 2016 Aug; 68(8): 1856-68. PMID: 26945549, DOI: 10.1002/art.39657, ISSN: 2326-5205.
Itani HA, McMaster WG, Saleh MA, Nazarewicz RR, Mikolajczyk TP, Kaszuba AM, Konior A, Prejbisz A, Januszewicz A, Norlander AE, Chen W, Bonami RH, Marshall AF, Poffenberger G, Weyand CM, Madhur MS, Moore DJ, Harrison DG, Guzik TJ. Activation of Human T Cells in Hypertension: Studies of Humanized Mice and Hypertensive Humans. Hypertension [print-electronic]. 2016 Jul; 68(1): 123-32. PMID: 27217403, PMCID: PMC4900908, PII: HYPERTENSIONAHA.116.07237, DOI: 10.1161/HYPERTENSIONAHA.116.07237, ISSN: 1524-4563.
Bonami RH, Thomas JW. Targeting Anti-Insulin B Cell Receptors Improves Receptor Editing in Type 1 Diabetes-Prone Mice. J. Immunol [print-electronic]. 2015 Nov 11/15/2015; 195(10): 4730-41. PMID: 26432895, PMCID: PMC4637270, PII: jimmunol.1500438, DOI: 10.4049/jimmunol.1500438, ISSN: 1550-6606.
Williams JM, Bonami RH, Hulbert C, Thomas JW. Reversing Tolerance in Isotype Switch-Competent Anti-Insulin B Lymphocytes. J. Immunol [print-electronic]. 2015 Aug 8/1/2015; 195(3): 853-64. PMID: 26109644, PMCID: PMC4506889, PII: jimmunol.1403114, DOI: 10.4049/jimmunol.1403114, ISSN: 1550-6606.
Case JB, Bonami RH, Nyhoff LE, Steinberg HE, Sullivan AM, Kendall PL. Bruton's Tyrosine Kinase Synergizes with Notch2 To Govern Marginal Zone B Cells in Nonobese Diabetic Mice. J. Immunol [print-electronic]. 2015 Jul 7/1/2015; 195(1): 61-70. PMID: 26034172, PMCID: PMC4551465, PII: jimmunol.1400803, DOI: 10.4049/jimmunol.1400803, ISSN: 1550-6606.
Bonami RH, Wolfle WT, Thomas JW, Kendall PL. NFATc2 (NFAT1) assists BCR-mediated anergy in anti-insulin B cells. Mol. Immunol [print-electronic]. 2014 Dec; 62(2): 321-8. PMID: 24507801, PMCID: PMC4125564, PII: S0161-5890(14)00012-1, DOI: 10.1016/j.molimm.2014.01.003, ISSN: 1872-9142.
Maseda D, Bonami RH, Crofford LJ. Regulation of B lymphocytes and plasma cells by innate immune mechanisms and stromal cells in rheumatoid arthritis. Expert Rev Clin Immunol [print-electronic]. 2014 Jun; 10(6): 747-62. PMID: 24734886, DOI: 10.1586/1744666X.2014.907744, ISSN: 1744-8409.
Bonami RH, Sullivan AM, Case JB, Steinberg HE, Hoek KL, Khan WN, Kendall PL. Bruton's tyrosine kinase promotes persistence of mature anti-insulin B cells. J. Immunol [print-electronic]. 2014 Feb 2/15/2014; 192(4): 1459-70. PMID: 24453243, PMCID: PMC4083749, PII: jimmunol.1300125, DOI: 10.4049/jimmunol.1300125, ISSN: 1550-6606.
Henry-Bonami RA, Williams JM, Rachakonda AB, Karamali M, Kendall PL, Thomas JW. B lymphocyte "original sin" in the bone marrow enhances islet autoreactivity in type 1 diabetes-prone nonobese diabetic mice. J. Immunol [print-electronic]. 2013 Jun 6/15/2013; 190(12): 5992-6003. PMID: 23677466, PMCID: PMC3679359, PII: jimmunol.1201359, DOI: 10.4049/jimmunol.1201359, ISSN: 1550-6606.
Henry RA, Kendall PL, Thomas JW. Autoantigen-specific B-cell depletion overcomes failed immune tolerance in type 1 diabetes. Diabetes [print-electronic]. 2012 Aug; 61(8): 2037-44. PMID: 22698916, PMCID: PMC3402296, PII: db11-1746, DOI: 10.2337/db11-1746, ISSN: 1939-327X.
Henry RA, Kendall PL. CXCL13 blockade disrupts B lymphocyte organization in tertiary lymphoid structures without altering B cell receptor bias or preventing diabetes in nonobese diabetic mice. J. Immunol [print-electronic]. 2010 Aug 8/1/2010; 185(3): 1460-5. PMID: 20574003, PMCID: PMC3824617, PII: jimmunol.0903710, DOI: 10.4049/jimmunol.0903710, ISSN: 1550-6606.
Henry RA, Kendall PL, Woodward EJ, Hulbert C, Thomas JW. Vkappa polymorphisms in NOD mice are spread throughout the entire immunoglobulin kappa locus and are shared by other autoimmune strains. Immunogenetics [print-electronic]. 2010 Aug; 62(8): 507-20. PMID: 20556377, PMCID: PMC2970566, DOI: 10.1007/s00251-010-0457-9, ISSN: 1432-1211.
Henry RA, Acevedo-Suárez CA, Thomas JW. Functional silencing is initiated and maintained in immature anti-insulin B cells. J. Immunol. 2009 Mar 3/15/2009; 182(6): 3432-9. PMID: 19265121, PMCID: PMC3845364, PII: 182/6/3432, DOI: 10.4049/jimmunol.0803121, ISSN: 1550-6606.
Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, Carter BD, Pozzi A, Abel TW, Dermody TS. Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe. 2009 Jan 1/22/2009; 5(1): 59-71. PMID: 19154988, PMCID: PMC2642927, PII: S1931-3128(08)00398-3, DOI: 10.1016/j.chom.2008.12.001, ISSN: 1934-6069.
Kramer KJ, Wilfong EM, Voss K, Barone SM, Shiakolas AR, Raju N, Roe CE, Suryadevara N, Walker L, Wall SC, Paulo A, Schaefer S, Dahunsi D, Westlake CS, Crowe JE, Carnahan RH, Rathmell JC, Bonami RH, Georgiev IS, Irish JM. Single-Cell Profiling of the Antigen-Specific Response to BNT162b2 SARS-CoV-2 RNA Vaccine. BioRxiv. 2021 Jul 7/28/2021; PMID: 34341788, PMCID: PMC8328055, DOI: 10.1101/2021.07.28.453981.
Young-Glazer J, Cisneros A, Wilfong EM, Smith SA, Crofford LJ, Bonami RH. Jo-1 autoantigen-specific B cells are skewed towards distinct functional B cell subsets in anti-synthetase syndrome patients. Arthritis Res Ther. 2021 Jan 1/19/2021; 23(1): 33. PMID: 33468230, PMCID: PMC7814460, PII: 10.1186/s13075-020-02412-8, DOI: 10.1186/s13075-020-02412-8, ISSN: 1478-6362.
Felton JL, Conway H, Bonami RH. B Quiet: Autoantigen-Specific Strategies to Silence Raucous B Lymphocytes and Halt Cross-Talk with T Cells in Type 1 Diabetes. Biomedicines. 2021 Jan 1/6/2021; 9(1): PMID: 33418839, PMCID: PMC7824835, PII: biomedicines9010042, DOI: 10.3390/biomedicines9010042, ISSN: 2227-9059.
Joosse BA, Jackson JH, Cisneros A, Santhin AB, Smith SA, Moore DJ, Crofford LJ, Wilfong EM, Bonami RH. High-Throughput Detection of Autoantigen-Specific B Cells Among Distinct Functional Subsets in Autoimmune Donors. Front Immunol. 2021; 12: 685718. PMID: 34234784, PMCID: PMC8256427, DOI: 10.3389/fimmu.2021.685718, ISSN: 1664-3224.
Bonami RH, Nyhoff LE, McNitt DH, Hulbert C, Felton JL, Kendall PL, Thomas JW. T-B Lymphocyte Interactions Promote Type 1 Diabetes Independently of SLAM-Associated Protein. J Immunol [print-electronic]. 2020 Dec 12/15/2020; 205(12): 3263-76. PMID: 33199538, PMCID: PMC7725913, PII: jimmunol.1900464, DOI: 10.4049/jimmunol.1900464, ISSN: 1550-6606.
Jackson MA, Bedingfield SK, Yu F, Stokan ME, Miles RE, Curvino EJ, Hoogenboezem EN, Bonami RH, Patel SS, Kendall PL, Giorgio TD, Duvall CL. Dual carrier-cargo hydrophobization and charge ratio optimization improve the systemic circulation and safety of zwitterionic nano-polyplexes. Biomaterials [print-electronic]. 2019 Feb; 192: 245-59. PMID: 30458360, PMCID: PMC6534819, PII: S0142-9612(18)30787-7, DOI: 10.1016/j.biomaterials.2018.11.010, ISSN: 1878-5905.
Wilson CS, Chhabra P, Marshall AF, Morr CV, Stocks BT, Hoopes EM, Bonami RH, Poffenberger G, Brayman KL, Moore DJ. Healthy Donor Polyclonal IgMs Diminish B-Lymphocyte Autoreactivity, Enhance Regulatory T-Cell Generation, and Reverse Type 1 Diabetes in NOD Mice. Diabetes [print-electronic]. 2018 Nov; 67(11): 2349-60. PMID: 30131391, PMCID: PMC6198348, PII: db18-0456, DOI: 10.2337/db18-0456, ISSN: 1939-327X.
Felton JL, Maseda D, Bonami RH, Hulbert C, Thomas JW. Anti-Insulin B Cells Are Poised for Antigen Presentation in Type 1 Diabetes. J. Immunol [print-electronic]. 2018 Aug 8/1/2018; 201(3): 861-73. PMID: 29950508, PII: jimmunol.1701717, DOI: 10.4049/jimmunol.1701717, ISSN: 1550-6606.
Nyhoff LE, Clark ES, Barron BL, Bonami RH, Khan WN, Kendall PL. Bruton's Tyrosine Kinase Is Not Essential for B Cell Survival beyond Early Developmental Stages. J. Immunol [print-electronic]. 2018 Apr 4/1/2018; 200(7): 2352-61. PMID: 29483358, PMCID: PMC6177684, PII: jimmunol.1701489, DOI: 10.4049/jimmunol.1701489, ISSN: 1550-6606.
Nyhoff LE, Barron BL, Johnson EM, Bonami RH, Maseda D, Fensterheim BA, Han W, Blackwell TS, Crofford LJ, Kendall PL. Bruton's Tyrosine Kinase Deficiency Inhibits Autoimmune Arthritis in Mice but Fails to Block Immune Complex-Mediated Inflammatory Arthritis. Arthritis & rheumatology (Hoboken, N.J.). 2016 Aug; 68(8): 1856-68. PMID: 26945549, DOI: 10.1002/art.39657, ISSN: 2326-5205.
Itani HA, McMaster WG, Saleh MA, Nazarewicz RR, Mikolajczyk TP, Kaszuba AM, Konior A, Prejbisz A, Januszewicz A, Norlander AE, Chen W, Bonami RH, Marshall AF, Poffenberger G, Weyand CM, Madhur MS, Moore DJ, Harrison DG, Guzik TJ. Activation of Human T Cells in Hypertension: Studies of Humanized Mice and Hypertensive Humans. Hypertension [print-electronic]. 2016 Jul; 68(1): 123-32. PMID: 27217403, PMCID: PMC4900908, PII: HYPERTENSIONAHA.116.07237, DOI: 10.1161/HYPERTENSIONAHA.116.07237, ISSN: 1524-4563.
Bonami RH, Thomas JW. Targeting Anti-Insulin B Cell Receptors Improves Receptor Editing in Type 1 Diabetes-Prone Mice. J. Immunol [print-electronic]. 2015 Nov 11/15/2015; 195(10): 4730-41. PMID: 26432895, PMCID: PMC4637270, PII: jimmunol.1500438, DOI: 10.4049/jimmunol.1500438, ISSN: 1550-6606.
Williams JM, Bonami RH, Hulbert C, Thomas JW. Reversing Tolerance in Isotype Switch-Competent Anti-Insulin B Lymphocytes. J. Immunol [print-electronic]. 2015 Aug 8/1/2015; 195(3): 853-64. PMID: 26109644, PMCID: PMC4506889, PII: jimmunol.1403114, DOI: 10.4049/jimmunol.1403114, ISSN: 1550-6606.
Case JB, Bonami RH, Nyhoff LE, Steinberg HE, Sullivan AM, Kendall PL. Bruton's Tyrosine Kinase Synergizes with Notch2 To Govern Marginal Zone B Cells in Nonobese Diabetic Mice. J. Immunol [print-electronic]. 2015 Jul 7/1/2015; 195(1): 61-70. PMID: 26034172, PMCID: PMC4551465, PII: jimmunol.1400803, DOI: 10.4049/jimmunol.1400803, ISSN: 1550-6606.
Bonami RH, Wolfle WT, Thomas JW, Kendall PL. NFATc2 (NFAT1) assists BCR-mediated anergy in anti-insulin B cells. Mol. Immunol [print-electronic]. 2014 Dec; 62(2): 321-8. PMID: 24507801, PMCID: PMC4125564, PII: S0161-5890(14)00012-1, DOI: 10.1016/j.molimm.2014.01.003, ISSN: 1872-9142.
Maseda D, Bonami RH, Crofford LJ. Regulation of B lymphocytes and plasma cells by innate immune mechanisms and stromal cells in rheumatoid arthritis. Expert Rev Clin Immunol [print-electronic]. 2014 Jun; 10(6): 747-62. PMID: 24734886, DOI: 10.1586/1744666X.2014.907744, ISSN: 1744-8409.
Bonami RH, Sullivan AM, Case JB, Steinberg HE, Hoek KL, Khan WN, Kendall PL. Bruton's tyrosine kinase promotes persistence of mature anti-insulin B cells. J. Immunol [print-electronic]. 2014 Feb 2/15/2014; 192(4): 1459-70. PMID: 24453243, PMCID: PMC4083749, PII: jimmunol.1300125, DOI: 10.4049/jimmunol.1300125, ISSN: 1550-6606.
Henry-Bonami RA, Williams JM, Rachakonda AB, Karamali M, Kendall PL, Thomas JW. B lymphocyte "original sin" in the bone marrow enhances islet autoreactivity in type 1 diabetes-prone nonobese diabetic mice. J. Immunol [print-electronic]. 2013 Jun 6/15/2013; 190(12): 5992-6003. PMID: 23677466, PMCID: PMC3679359, PII: jimmunol.1201359, DOI: 10.4049/jimmunol.1201359, ISSN: 1550-6606.
Henry RA, Kendall PL, Thomas JW. Autoantigen-specific B-cell depletion overcomes failed immune tolerance in type 1 diabetes. Diabetes [print-electronic]. 2012 Aug; 61(8): 2037-44. PMID: 22698916, PMCID: PMC3402296, PII: db11-1746, DOI: 10.2337/db11-1746, ISSN: 1939-327X.
Henry RA, Kendall PL. CXCL13 blockade disrupts B lymphocyte organization in tertiary lymphoid structures without altering B cell receptor bias or preventing diabetes in nonobese diabetic mice. J. Immunol [print-electronic]. 2010 Aug 8/1/2010; 185(3): 1460-5. PMID: 20574003, PMCID: PMC3824617, PII: jimmunol.0903710, DOI: 10.4049/jimmunol.0903710, ISSN: 1550-6606.
Henry RA, Kendall PL, Woodward EJ, Hulbert C, Thomas JW. Vkappa polymorphisms in NOD mice are spread throughout the entire immunoglobulin kappa locus and are shared by other autoimmune strains. Immunogenetics [print-electronic]. 2010 Aug; 62(8): 507-20. PMID: 20556377, PMCID: PMC2970566, DOI: 10.1007/s00251-010-0457-9, ISSN: 1432-1211.
Henry RA, Acevedo-Suárez CA, Thomas JW. Functional silencing is initiated and maintained in immature anti-insulin B cells. J. Immunol. 2009 Mar 3/15/2009; 182(6): 3432-9. PMID: 19265121, PMCID: PMC3845364, PII: 182/6/3432, DOI: 10.4049/jimmunol.0803121, ISSN: 1550-6606.
Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, Carter BD, Pozzi A, Abel TW, Dermody TS. Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe. 2009 Jan 1/22/2009; 5(1): 59-71. PMID: 19154988, PMCID: PMC2642927, PII: S1931-3128(08)00398-3, DOI: 10.1016/j.chom.2008.12.001, ISSN: 1934-6069.