Noah Butler, PhD

Portrait
Associate Professor of Microbiology and Immunology
Member
Member
Member

Contact Information

Primary Office
3-632 Bowen Science Building
51 Newton Rd
Iowa City, IA 52242
319-335-7789

Lab
3-615D Bowen Science Building
51 Newton Rd
Iowa City, IA 52242
319-335-7938

Education

BS, Biological Sciences, University of Iowa
MHS, Immunology, Johns Hopkins Bloomberg School of Public Health
PhD, Immunology, University of Iowa
Postdoctoral Fellow, Immunology, Department of Microbiology, University of Iowa

Education/Training Program Affiliations

Biomedical Science Program, Department of Microbiology Graduate Program, Medical Scientist Training Program

Research Summary

Malaria remains a global heath crisis with billions of people at risk for developing this disease each year.

Our research is focused on understanding how the function of Plasmodium parasite-specific B cells and T cells are regulated during malaria. Our broader goals are to use this information to identify and develop new strategies to improve immunity against this globally important disease.

To achieve our goals, we are performing experiments designed to elucidate the molecular and transcriptional mechanisms that determine how infection, inflammation and immunotherapy impact the formation of long-lived, pathogen-specific memory T cell and B cell subsets.

As part of our efforts, we also perform comprehensive, comparative studies using models of vaccination, bacterial and viral infection, and we investigate host immunity using related eukaryotic pathogens.

Publications

Hahn, W. O., Butler, N. S., Lindner, S. E., Sather, D. N., Kappe, S. H., Hamerman, J. A., Gale, M., Liles, W. C. & Pepper, M. (2018). cGAS-mediated control of blood stage malaria promotes Plasmodium-specific germinal center responses. JCI Insight. DOI: 10.1172/jci.insight.94142.

Smith, L. K., Boukhaled, G. M., Condotta, S. A., Mazouz, S., Guthmiller, J. C., Vijay, R., Butler, N. S., Bruneau, J., Shoukry, N. H., Krawczyk, C. M. & Richer, M. J. (2018). Interleukin-10 Directly Inhibits CD8+T Cell Function by Enhancing N-Glycan Branching to Decrease Antigen Sensitivity. Immunity, 48, 1-14. DOI: doi.org/10.1016/j.immuni.2018.01.006.

Zander, R. A., Vijay, R., Pack, A. D., Guthmiller, J. J., Graham, A. C., Lindner, S. E., Vaughan, A. M., Kappe, S. H. & Butler, N. S. (2017). Th1-like Plasmodium-Specific Memory CD4+ T Cells Support Humoral Immunity. Cell Reports. PMID: 29141217.

Rivera-Correa, J., Guthmiller, J. J., Vijay, R., Fernandez-Arias, C., Pardo-Ruge, M. A., Butler, N. S., Gonzalez, S. & Rodriguez, A. (2017). Plasmodium DNA-mediated TLR9 activation of T-bet+ B cells contributes to autoimmune anaemia during malaria. Nature Communications, 1(8), 1282. PMID: 29101363.

Kurup, S. A., Obeng-Adjei, N., Anthony, S. M., Traore, B., Doumbo, O. K., Butler, N. S., Crompton, P. D. & Harty, J. T. (2017). Regulatory T cells impede acute and long-term immunity to blood stage malaria through CTLA-4. Nature Medicine. PMID: 28892065.

Niu, G., Franca, C., Roobsoong, W., Nguitragool, W., Wang, X., Prachumsri, J., Butler, N. S. & Li, J. (2017). Fibrinogen domain of FREP1 is a broad spectrum malaria transmission-blocking vaccine antigen. Journal of Biological Chemistry, 292(28), 11960-11969. PMID: 28533429.

Huggins, M. A., Johnson, H. L., Jin, F., N'Songo, A., Hanson, L. M., LaFrance, S. J., Butler, N. S., Harty, J. T. & Johnson, A. J. (2017). Perforin Expression by CD8 T Cells Is Sufficient To Cause Fatal Brain Edema during Experimental Cerebral Malaria. Infect Immun, 85(5), e00985-16. PMID: 28264905.

Guthmiller, J. J., Graham, A. C., Zander, R. A., Pope, R. L. & Butler, N. S. (2017). Cutting Edge: IL-10 Is Essential for the Generation of Germinal Center B Cell Responses and Anti-Plasmodium Humoral Immunity. J Immunol, 198(2), 617-22. PMID: 27940658.

Zander, R. A., Guthmiller, J. J., Graham, A. C., Pope, R. L., Burke, B. E., Carr, D. J. & Butler, N. S. (2016). Type I Interferons Induce T Regulatory 1 Responses and Restrict Humoral Immunity during Experimental Malaria. PLoS Pathog, 12(10), e1005945. PMID: 27732671.

Richer, M. J., Lang, M. L. & Butler, N. S. (2016). T Cell Fates Zipped Up: How the Bach2 Basic Leucine Zipper Transcriptional Repressor Directs T Cell Differentiation and Function. J Immunol, 197(4), 1009-15. PMID: 27496973.

Butler, N. S., Schmidt, N. W. (2015). Erythropoietin-producing hepatocellular receptor B2 receptor tyrosine kinase: A novel regulator of infection- and inflammation-induced liver fibrosis. (Vols. 62). (3), pp. 680-3. Hepatology. PMID: 25914283.

Zhang, G., Niu, G., Franca, C. M., Dong, Y., Wang, X., Butler, N. S., Dimopoulos, G. & Li, J. (2015). Anopheles Midgut FREP1 Mediates Plasmodium Invasion. J Biol Chem, 290(27), 16490-501. PMID: 25991725.

Butler, N. S., Kulu, D. I. (2015). The regulation of T follicular helper responses during infection. Curr Opin Immunol, 34, 68-74. PMID: 25726751.

Zander, R. A., Obeng-Adjei, N., Guthmiller, J. J., Kulu, D. I., Li, J., Ongoiba, A., Traore, B., Crompton, P. D. & Butler, N. S. (2015). PD-1 Co-inhibitory and OX40 Co-stimulatory Crosstalk Regulates Helper T Cell Differentiation and Anti-Plasmodium Humoral Immunity. Cell Host Microbe, 17(5), 628-41. PMID: 25891357.

Guthmiller, J. J., Zander, R. A. & Butler, N. S. (2015). Measurement of the T Cell Response to Preerythrocytic Vaccination in Mice. In Methods Mol Biol. pp. 19-37. PMID: 26450376.

Trujillo, J. A., Croft, N. P., Dudek, N. L., Channappanavar, R., Theodossis, A., Webb, A. I., Dunstone, M. A., Illing, P. T., Butler, N. S., Fett, C., Tscharke, D. C., Rossjohn, J., Perlman, S. & Purcell, A. W. (2014). The cellular redox environment alters antigen presentation. J Biol Chem, 289(40), 27979-91. PMID: 25135637.

Doll, K. L., Butler, N. S. & Harty, J. T. (2014). CD8 T cell independent immunity after single dose infection-treatment-vaccination (ITV) against Plasmodium yoelii. Vaccine, 32(4), 483-91. PMID: 24321740.

Butler, N. S., Harris, T. H. & Blader, I. J. (2013). Regulation of immunopathogenesis during Plasmodium and Toxoplasma infections: more parallels than distinctions?. Trends Parasitol, 29(12), 593-602. PMID: 24184186.

Zander, R. A., Butler, N. S. (2013). Dysfunctional adaptive immunity during parasitic infections. Curr Immunol Rev, 9(3), 179-89. PMID: 24839433.

Illingworth, J., Butler, N. S., Roetynck, S., Mwacharo, J., Pierce, S. K., Bejon, P., Crompton, P. D., Marsh, K. & Ndungu, F. M. (2013). Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J Immunol, 190(3), 1038-47. PMID: 23264654.

Doll, K. L., Butler, N. S. & Harty, J. T. (2013). Tracking the total CD8 T cell response following whole Plasmodium vaccination. Methods Mol Biol, 923, 493-504. PMID: 22990800.

Butler, N. S. (2013). Vaccination Against Malaria Parasites: Paradigms, Perils and Progress. In M. Geist (Eds.) Molecular Vaccines-From Prophylaxis to Therapy. Vienna: Springer Press.

Butler, N. S., Vaughan, A. M., Harty, J. T. & Kappe, S. H. (2012). Whole parasite vaccination approaches for prevention of malaria infection. Trends Immunol, 33(5), 247-54. PMID: 22405559.

Butler, N. S., Moebius, J., Pewe, L. L., Traore, B., Doumbo, O. K., Tygrett, L. T., Waldschmidt, T. J., Crompton, P. D. & Harty, J. T. (2011). Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nat Immunol, 13(2), 188-95. PMID: 22157630.

Butler, N. S., Nolz, J. C. & Harty, J. T. (2011). Immunologic considerations for generating memory CD8 T cells through vaccination. Cell Microbiol, 13(7), 925-33. PMID: 21501363.

Butler, N. S., Schmidt, N. W., Vaughan, A. M., Aly, A. S., Kappe, S. H. & Harty, J. T. (2011). Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe, 9(6), 451-62. PMID: 21669394.

Schmidt, N. W., Butler, N. S. & Harty, J. T. (2011). Plasmodium-host interactions directly influence the threshold of memory CD8 T cells required for protective immunity. J Immunol, 186(10), 5873-84. PMID: 21460205.

Schmidt, N. W., Butler, N. S., Badovinac, V. P. & Harty, J. T. (2010). Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS Pathog, 6(7), e1000998. PMID: 20657824.

Butler, N. S., Schmidt, N. W. & Harty, J. T. (2010). Differential effector pathways regulate memory CD8 T cell immunity against Plasmodium berghei versus P. yoelii sporozoites. J Immunol, 184(5), 2528-38. PMID: 20097864.

Butler, N. S., Harty, J. T. (2010). The role of inflammation in the generation and maintenance of memory T cells. In Adv Exp Med Biol. pp. 42-56. PMID: 20795539.

Schmidt, N. W., Butler, N. S. & Harty, J. T. (2009). CD8 T cell immunity to Plasmodium permits generation of protective antibodies after repeated sporozoite challenge. Vaccine, 27(44), 6103-6. PMID: 19712771.

Butler, N. S., Harty, J. T. (2009). A "memorable" NK cell discovery. (Vols. 19). (3), pp. 277-8. Cell Res. PMID: 19252510.

Butler, N. S., Theodossis, A., Webb, A. I., Nastovska, R., Ramarathinam, S. H., Dunstone, M. A., Rossjohn, J., Purcell, A. W. & Perlman, S. (2008). Prevention of cytotoxic T cell escape using a heteroclitic subdominant viral T cell determinant. PLoS Pathog, 4(10), e1000186. PMID: 18949029.

Schmidt, N. W., Podyminogin, R. L., Butler, N. S., Badovinac, V. P., Tucker, B. J., Bahjat, K. S., Lauer, P., Reyes-Sandoval, A., Hutchings, C. L., Moore, A. C., Gilbert, S. C., Hill, A. V., Bartholomay, L. C. & Harty, J. T. (2008). Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc Natl Acad Sci U S A, 105(37), 14017-22. PMID: 18780790.

Butler, N. S., Theodossis, A., Webb, A. I., Dunstone, M. A., Nastovska, R., Ramarathinam, S. H., Rossjohn, J., Purcell, A. W. & Perlman, S. (2008). Structural and biological basis of CTL escape in coronavirus-infected mice. J Immunol, 180(6), 3926-37. PMID: 18322201.

Butler, N. S., Dandekar, A. A. & Perlman, S. (2007). Antiviral antibodies are necessary to prevent cytotoxic T-lymphocyte escape in mice infected with a coronavirus. J Virol, 81(24), 13291-8. PMID: 17913802.

Yarovinsky, T. O., Butler, N. S., Monick, M. M. & Hunninghake, G. W. (2006). Early exposure to IL-4 stabilizes IL-4 mRNA in CD4+ T cells via RNA-binding protein HuR. J Immunol, 177(7), 4426-35. PMID: 16982877.

Butler, N., Pewe, L., Trandem, K. & Perlman, S. (2006). Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology, 347(2), 410-21. PMID: 16413043.

Perlman, S., Butler, N. (2006). Neurotropic coronavirus infections. In C. S. Reiss (Eds.) Neurotropic Viral Infections. New York: Cambridge University Press.

Ashare, A., Powers, L. S., Butler, N. S., Doerschug, K. C., Monick, M. M. & Hunninghake, G. W. (2005). Anti-inflammatory response is associated with mortality and severity of infection in sepsis. Am J Physiol Lung Cell Mol Physiol, 288(4), L633-40. PMID: 15579629.

Monick, M. M., Cameron, K., Powers, L. S., Butler, N. S., McCoy, D., Mallampalli, R. K. & Hunninghake, G. W. (2004). Sphingosine kinase mediates activation of extracellular signal-related kinase and Akt by respiratory syncytial virus. Am J Respir Cell Mol Biol, 30(6), 844-52. PMID: 14742298.

Monick, M. M., Yarovinsky, T. O., Powers, L. S., Butler, N. S., Carter, A. B., Gudmundsson, G. & Hunninghake, G. W. (2003). Respiratory syncytial virus up-regulates TLR4 and sensitizes airway epithelial cells to endotoxin. J Biol Chem, 278(52), 53035-44. PMID: 14565959.

Monick, M. M., Samavati, L., Butler, N. S., Mohning, M., Powers, L. S., Yarovinski, T., Spitz, D. R. & Hunninghake, G. W. (2003). Intracellular thiols contribute to Th2 function via a positive role in IL-4 production. J Immunol, 171(10), 5107-15. PMID: 14607909.

Nyunoya, T., Powers, L. S., Yarovinsky, T. O., Butler, N. S., Monick, M. M. & Hunninghake, G. W. (2003). Hyperoxia induces macrophage cell cycle arrest by adhesion-dependent induction of p21Cip1 and activation of the retinoblastoma protein. J Biol Chem, 278(38), 36099-106. PMID: 12847100.

Monick, M. M., Powers, L. S., Butler, N. S. & Hunninghake, G. W. (2003). Inhibition of Rho family GTPases results in increased TNF-alpha production after lipopolysaccharide exposure. J Immunol, 171(5), 2625-30. PMID: 12928415.

Yarovinsky, T. O., Powers, L. S., Butler, N. S., Bradford, M. A., Monick, M. M. & Hunninghake, G. W. (2003). Adenoviral infection decreases mortality from lipopolysaccharide-induced liver failure via induction of TNF-alpha tolerance. J Immunol, 171(5), 2453-60. PMID: 12928393.

Chung, M. P., Monick, M. M., Hamzeh, N. Y., Butler, N. S., Powers, L. S. & Hunninghake, G. W. (2003). Role of repeated lung injury and genetic background in bleomycin-induced fibrosis. Am J Respir Cell Mol Biol, 29(3 Pt 1), 375-80. PMID: 12676806.

Butler, N. S., Monick, M. M., Yarovinsky, T. O., Powers, L. S. & Hunninghake, G. W. (2002). Altered IL-4 mRNA stability correlates with Th1 and Th2 bias and susceptibility to hypersensitivity pneumonitis in two inbred strains of mice. J Immunol, 169(7), 3700-9. PMID: 12244163.

Monick, M. M., Robeff, P. K., Butler, N. S., Flaherty, D. M., Carter, A. B., Peterson, M. W. & Hunninghake, G. W. (2002). Phosphatidylinositol 3-kinase activity negatively regulates stability of cyclooxygenase 2 mRNA. J Biol Chem, 277(36), 32992-3000. PMID: 12072439.

Monick, M. M., Powers, L., Butler, N., Yarovinsky, T. & Hunninghake, G. W. (2002). Interaction of matrix with integrin receptors is required for optimal LPS-induced MAP kinase activation. Am J Physiol Lung Cell Mol Physiol, 283(2), L390-402. PMID: 12114201.

Sanlioglu, S., Williams, C. M., Samavati, L., Butler, N. S., Wang, G., McCray, P. B., Ritchie, T. C., Hunninghake, G. W., Zandi, E. & Engelhardt, J. F. (2001). Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem, 276(32), 30188-98. PMID: 11402028.

Millá, E., Héon, E., Piguet, B., Ducrey, N., Butler, N., Stone, E., Schorderet, D. F. & Munier, F. (1998). Mutational screening of peripherin/RDS genes, rhodopsin and ROM-1 in 69 index cases with retinitis pigmentosa and other retinal dystrophies. Klin Monbl Augenheilkd, 212(5), 305-8. PMID: 9677563.

Weleber, R. G., Butler, N. S., Murphey, W. H., Sheffield, V. C. & Stone, E. M. (1997). X-linked retinitis pigmentosa associated with a 2-base pair insertion in codon 99 of the RP3 gene RPGR. Arch Ophthalmol, 115(11), 1429-35. PMID: 9366675.

Fishman, G. A., Stone, E. M., Alexander, K. R., Gilbert, L. D., Derlacki, D. J. & Butler, N. S. (1997). Serine-27-phenylalanine mutation within the peripherin/RDS gene in a family with cone dystrophy. Ophthalmology, 104(2), 299-306. PMID: 9052636.

Piguet, B., Héon, E., Munier, F. L., Grounauer, P. A., Niemeyer, G., Butler, N., Schorderet, D. F., Sheffield, V. C. & Stone, E. M. (1996). Full characterization of the maculopathy associated with an Arg-172-Trp mutation in the RDS/peripherin gene. Ophthalmic Genet, 17(4), 175-86. PMID: 9010868.