Education

Biography

Helder Nakaya is an assistant professor at the University of São Paulo, Brazil. His lab is focused on investigating the basis of infectious diseases using computational systems biology. He is also an adjunct professor at Emory University School of Medicine, USA. With a PhD in Molecular Biology and extensive training in Bioinformatics, he became an expert in Systems Vaccinology, an interdisciplinary field that combines systems-wide measurements, networks, and predictive modeling in the context of vaccines and infectious disease. Dr. Nakaya has developed systems biology approaches to understand and predict the mechanisms of vaccine induced-immunity for Yellow Fever, seasonal Influenza, Meningococcal, Shingles, malaria, and Tularemia vaccines.

Research Interest

1. Systems Biology
2. Computational tools
3. Transcriptional Regulatory Mechanisms

Scientific Activities

Publications

Refereed Journals

1. Li S, Sullivan NL, Rouphael N, Yu T, Banton S, Maddur MS, McCausland M, Chiu C, Canniff J, Dubey S, Liu K, Tran V, Hagan T, Duraisingham S, Wieland A, Mehta A, Whitaker J, Subramaniam S, Jones DP, Sette A, Vora K, Weinberg A, Mulligan MJ, Nakaya HI, Levin M, Ahmed R, Pulendran B. Metabolic Phenotypes of Response to Vaccination in Humans. CELL, 2017 May 18;169(5):862-877.e17.
2. Prada-Medina CA, Fukutani KF, Kumar NP, Gil-Santana L, Babu S, Lichtenstein F, West K, Sivakumar S, Menon PA, Viswanathan V, Andrade BB, Nakaya HI, Kornfeld H. Systems Immunology of Diabetes-Tuberculosis Comorbidity Reveals Signatures of Disease Complications. ScientificReports, 2017 May 17;7(1):1999
3. Costa VV, Del Sarto JL, Rocha RF, Silva FR, Doria JG, Olmo IG, Marques RE,Queiroz-Junior CM, Foureaux G, Araújo JMS, Cramer A, Real ALCV, Ribeiro LS, Sardi SI, Ferreira AJ, Machado FS, de Oliveira AC, Teixeira AL, Nakaya HI, Souza DG, Ribeiro FM, Teixeira MM. N-Methyl-d-Aspartate (NMDA) Receptor Blockade Prevents Neuronal Death Induced by Zika Virus Infection. MBio. 2017 Apr 25;8(2). pii: e00350-17.
4. Kazmin D, Nakaya HI, Lee EK, Johnson MJ, van der Most R, van den Berg RA, Ballou WR, Jongert E, Wille-Reece U, Ockenhouse C, Aderem A, Zak DE, Sadoff J, Hendriks J, Wrammert J, Ahmed R, Pulendran B. Systems analysis of protective immune responses to RTS,S malaria vaccination in humans. PNAS. 2017 Feb 28;114(9):2425-2430.
5. Geraldo MV, Nakaya HI, Kimura ET. Down-regulation of 14q32-encoded miRNAs and tumor suppressor role for miR-654-3p in papillary thyroid cancer. Oncotarget. 2017 Feb 7;8(6):9597-9607.
6. Ferreira LR, Ferreira FM, Nakaya HI, Deng X, Cândido DD, de Oliveira LC, Billaud JN, Lanteri MC, Rigaud VO, Seielstad M, Kalil J, Fernandes F, Ribeiro AL, Sabino EC, Cunha-Neto E. Blood Gene Signatures of Chagas Cardiomyopathy With or Without Ventricular Dysfunction. J Infect Dis. 2017 Feb 1;215(3):387-395.
7. Muñoz M, Craske M, Severino P, de Lima TM, Labhart P, Chammas R, Velasco IT, Machado MC, Egan B, Nakaya HI, Pinheiro da Silva F. Antimicrobial peptide LL-37 participates in the transcriptional regulation of melanoma cells. J Cancer. 2016 Nov 26;7(15):2341-2345.
8. Kasturi SP, Kozlowski PA, Nakaya HI, Burger MC, Russo P, Pham M, Kovalenkov Y, Silveira EL, Havenar-Daughton C, Burton SL, Kilgore KM, Johnson MJ, Nabi R, Legere T, Sher ZJ, Chen X, Amara RR, Hunter E, Bosinger SE, Spearman P, Crotty S, Villinger F, Derdeyn CA, Wrammert J, Pulendran B. Adjuvanting a Simian Immunodeficiency Virus Vaccine with Toll-Like Receptor Ligands Encapsulated in Nanoparticles Induces Persistent Antibody Responses and Enhanced Protection in TRIM5α Restrictive Macaques. J Virol. 2017 Jan 31;91(4). pii: e01844-16.
9. Lever M, Silveira EL, Nakaya HI. Systems Vaccinology Applied to DNA Vaccines: Perspective and Challenges. Curr Issues Mol Biol. 2017;22:1-16.
10. Ellebedy AH, Jackson KJ, Kissick HT, Nakaya HI, Davis CW, Roskin KM, McElroy AK, Oshansky CM, Elbein R, Thomas S, Lyon GM, Spiropoulou CF, Mehta AK, Thomas PG, Boyd SD, Ahmed R. Defining antigen-specific plasmablast and memory B cell subsets in human blood after viral infection or vaccination. Nature Immunology. 2016 Oct;17(10):1226-34.
11. Im SJ, Hashimoto M, Gerner MY, Lee J, Kissick HT, Burger MC, Shan Q, Hale JS, Lee J, Nasti TH, Sharpe AH, Freeman GJ, Germain RN, Nakaya HI, Xue HH, Ahmed R. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature. 2016 Sep 15;537(7620):417-421.
12. Schroder WA, Anraku I, Le TT, Hirata TD, Nakaya HI, Major L, Ellis JJ, Suhrbier A. SerpinB2 Deficiency Results in a Stratum Corneum Defect and Increased Sensitivity to Topically Applied Inflammatory Agents. Am J Pathol. 2016 Jun;186(6):1511-23.
13. Ravindran R, Loebbermann J, Nakaya HI, Khan N, Ma H, Gama L, Machiah DK, Lawson B, Hakimpour P, Wang YC, Li S, Sharma P, Kaufman RJ, Martinez J, Pulendran B. The amino acid sensor GCN2 controls gut inflammation by inhibiting inflammasome activation. Nature. 2016 Mar 24;531(7595):523-7.
14. Schons-Fonseca L, da Silva JB, Milanez JS, Domingos RH, Smith JL, Nakaya HI, Grossman AD, Ho PL, da Costa RM. Analysis of LexA binding sites and transcriptomics in response to genotoxic stress in Leptospira interrogans. Nucleic Acids Res. 2016 Feb 18;44(3):1179-91.
15. Nakaya HI, Clutterbuck E, Kazmin D, Wang L, Cortese M, Bosinger SE, Patel NB, Zak DE, Aderem A, Dong T, Del Giudice G, Rappuoli R, Cerundolo V, Pollard AJ, Pulendran B, Siegrist CA. Systems biology of immunity to MF59-adjuvanted versus nonadjuvanted trivalent seasonal influenza vaccines in early childhood. PNAS. 2016 Feb 16;113(7):1853-8.
16. Nakaya HI, Hagan T, Duraisingham SS, Lee EK, Kwissa M, Rouphael N, FrascaD, Gersten M, Mehta AK, Gaujoux R, Li GM, Gupta S, Ahmed R, Mulligan MJ, Shen-Orr S, Blomberg BB, Subramaniam S, Pulendran B. Systems Analysis of Immunity to Influenza Vaccination across Multiple Years and in Diverse Populations Reveals Shared Molecular Signatures. Immunity. 2015 Dec 15;43(6):1186-98.
17. Okada SS, de Oliveira EM, de Araújo TH, Rodrigues MR, Albuquerque RC, Mortara RA, Taniwaki NN, Nakaya HI, Campa A, Moreno AC. Myeloperoxidase in human peripheral blood lymphocytes: Production and subcellular localization. Cell Immunol. 2016 Feb;300:18-25.
18. Almeida GT, Lage RC, Anderson L, Venancio TM, Nakaya HI, Miyasato PA, Rofatto HK, Zerlotini A, Nakano E, Oliveira G, Verjovski-Almeida S. Synergy of Omeprazole and Praziquantel In Vitro Treatment against Schistosoma mansoni Adult Worms. PLoSNegl Trop Dis. 2015 Sep 24;9(9):e0004086.
19. Uren PJ, Vo DT, de Araujo PR, Pötschke R, Burns SC, Bahrami-Samani E, Qiao M, de Sousa Abreu R, Nakaya HI, Correa BR, Kühnöl C, Ule J, Martindale JL, Abdelmohsen K, Gorospe M, Smith AD, Penalva LO. RNA-Binding Protein Musashi1 Is a Central Regulator of Adhesion Pathways in Glioblastoma. Mol Cell Biol. 2015 Sep 1;35(17):2965-78.
20. Navarro IC, Ferreira FM, Nakaya HI, Baron MA, Vilar-Pereira G, Pereira IR, Silva AM, Real JM, De Brito T, Chevillard C, Lannes-Vieira J, Kalil J, Cunha-Neto E, Ferreira LR. MicroRNA Transcriptome Profiling in Heart of Trypanosoma cruzi-Infected Mice: Parasitological and Cardiological Outcomes. PLoSNegl Trop Dis. 2015 Jun 18;9(6):e0003828.
21. Nakaya HI, Pulendran B. Vaccinology in the era of high-throughput biology. Philos Trans R SocLond B Biol Sci. 2015 Jun 19;370(1671). pii: 20140146.
22. Nakaya HI, Bruna-Romero O. Is the gut microbiome key to modulating vaccine efficacy? Expert Rev Vaccines. 2015 Jun;14(6):777-9.
23. Hagan T, Nakaya HI, Subramaniam S, Pulendran B. Systems vaccinology: Enabling rational vaccine design with systems biological approaches. Vaccine. 2015 Sep 29;33(40):5294-301.
24. Akondy RS, Johnson PL, Nakaya HI, Edupuganti S, Mulligan MJ, Lawson B, Miller JD, Pulendran B, Antia R, Ahmed R. Initial viral load determines the magnitude of the human CD8 T cell response to yellow fever vaccination. PNAS. 2015 Mar 10;112(10):3050-5.
25. Poo YS, Rudd PA, Gardner J, Wilson JA, Larcher T, Colle MA, Le TT, Nakaya HI, Warrilow D, Allcock R, Bielefeldt-Ohmann H, Schroder WA, Khromykh AA, Lopez JA, Suhrbier A. Multiple immune factors are involved in controlling acute and chronic chikungunya virus infection. PLoSNegl Trop Dis. 2014 Dec 4;8(12):e3354.
26. Oh JZ, Ravindran R, Chassaing B, Carvalho FA, Maddur MS, Bower M, Hakimpour P, Gill KP, Nakaya HI, Yarovinsky F, Sartor RB, Gewirtz AT, Pulendran B. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity. 2014 Sep 18;41(3):478-92.
27. Kwissa M, Nakaya HI, Onlamoon N, Wrammert J, Villinger F, Perng GC, Yoksan S, Pattanapanyasat K, Chokephaibulkit K, Ahmed R, Pulendran B. Dengue virus infection induces expansion of a CD14(+)CD16(+) monocyte population that stimulates plasmablast differentiation. Cell Host Microbe. 2014 Jul 9;16(1):115-27.
28. Poo YS, Nakaya H, Gardner J, Larcher T, Schroder WA, Le TT, Major LD, Suhrbier A. CCR2 deficiency promotes exacerbated chronic erosive neutrophil-dominated chikungunya virus arthritis. J Virol. 2014 Jun;88(12):6862-72.
29. Medina-Acosta E, Nakaya HT, Pontillo A, de Souza Campos Fernandes RC. Genetic control of immune response and susceptibility to infectious diseases. Biomed Res Int. 2014;2014:796073.
30. Tamim S, Vo DT, Uren PJ, Qiao M, Bindewald E, Kasprzak WK, Shapiro BA, Nakaya HI, Burns SC, Araujo PR, Nakano I, Radek AJ, Kuersten S, Smith AD, Penalva LO. Genomic analyses reveal broad impact of miR-137 on genes associated with malignant transformation and neuronal differentiation in glioblastoma cells. PLoS One. 2014 Jan 22;9(1):e85591.
31. Li S, Rouphael N, Duraisingham S, Romero-Steiner S, Presnell S, Davis C, Schmidt DS, Johnson SE, Milton A, Rajam G, Kasturi S, Carlone GM, Quinn C, Chaussabel D, Palucka AK, Mulligan MJ, Ahmed R, Stephens DS, Nakaya HI, Pulendran B. Molecular signatures of antibody responses derived from a systems biology study of five human vaccines. Nature Immunology. 2014 Feb;15(2):195-204.
32. Ravindran R, Khan N, Nakaya HI, Li S, Loebbermann J, Maddur MS, Park Y, Jones DP, Chappert P, Davoust J, Weiss DS, Virgin HW, Ron D, Pulendran B. Vaccine activation of the nutrient sensor GCN2 in dendritic cells enhances antigen presentation. Science. 2014 Jan 17;343(6168):313-7.
33. Tan Y, Tamayo P, Nakaya H, Pulendran B, Mesirov JP, Haining WN. Gene signatures related to B-cell proliferation predict influenza vaccine-induced antibody response. Eur J Immunol. 2014 Jan;44(1):285-95.
34. Beckedorff FC, Ayupe AC, Crocci-Souza R, Amaral MS, Nakaya HI, Soltys DT, Menck CF, Reis EM, Verjovski-Almeida S. The intronic long noncoding RNA ANRASSF1 recruits PRC2 to the RASSF1A promoter, reducing the expression of RASSF1A and increasing cell proliferation. PLoSGenet. 2013;9(8):e1003705.
35. Pulendran B, Oh JZ, Nakaya HI, Ravindran R, Kazmin DA. Immunity to viruses: learning from successful human vaccines. Immunol Rev. 2013 Sep;255(1):243-55.
36. Li S, Nakaya HI, Kazmin DA, Oh JZ, Pulendran B. Systems biological approaches to measure and understand vaccine immunity in humans. Semin Immunol. 2013 Oct 31;25(3):209-18.
37. Varani AM, Monteiro-Vitorello CB, Nakaya HI, Van Sluys MA. The role of prophage in plant-pathogenic bacteria. Annu Rev Phytopathol. 2013;51:429-51.
38. Norris BA, Uebelhoer LS, Nakaya HI, Price AA, Grakoui A, Pulendran B. Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity. 2013 Feb 21;38(2):309-21.
39. Nakaya HI, Gardner J, Poo YS, Major L, Pulendran B, Suhrbier A. Gene profiling of Chikungunya virus arthritis in a mouse model reveals significant overlap with rheumatoid arthritis. Arthritis Rheum. 2012 Nov;64(11):3553-63.
40. Jones CL, Sampson TR, Nakaya HI, Pulendran B, Weiss DS. Repression of bacterial lipoprotein production by Francisellanovicida facilitates evasion of innate immune recognition. Cell Microbiol. 2012 Oct;14(10):1531-43.
41. Kwissa M, Nakaya HI, Oluoch H, Pulendran B. Distinct TLR adjuvants differentially stimulate systemic and local innate immune responses in nonhuman primates. Blood. 2012 Mar 1;119(9):2044-55.
42. Nakaya HI, Pulendran B. Systems vaccinology: its promise and challenge for HIV vaccine development. CurrOpin HIV AIDS. 2012 Jan;7(1):24-31.
43. Nakaya HI, Li S, Pulendran B. Systems vaccinology: learning to compute the behavior of vaccine induced immunity. Wiley Interdiscip Rev SystBiol Med. 2012 Mar-Apr;4(2):193-205.
44. Nakaya HI, Wrammert J, Lee EK, Racioppi L, Marie-Kunze S, Haining WN, Means AR, Kasturi SP, Khan N, Li GM, McCausland M, Kanchan V, Kokko KE, Li S, Elbein R, Mehta AK, Aderem A, Subbarao K, Ahmed R, Pulendran B. Systems biology of vaccination for seasonal influenza in humans. Nature Immunology. 2011 Jul 10;12(8):786-95.
45. Duraiswamy J, Ibegbu CC, Masopust D, Miller JD, Araki K, Doho GH, Tata P, Gupta S, Zilliox MJ, Nakaya HI, Pulendran B, Haining WN, Freeman GJ, Ahmed R. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J Immunol. 2011 Apr 1;186(7):4200-12.
46. Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, Ravindran R, Stewart S, Alam M, Kwissa M, Villinger F, Murthy N, Steel J, Jacob J, Hogan RJ, García-Sastre A, Compans R, Pulendran B. Programming the magnitude and persistence of antibody responses with innate immunity. Nature. 2011 Feb 24;470(7335):543-7.
47. Pulendran B, Li S, Nakaya HI. Systems vaccinology. Immunity. 2010 Oct 29;33(4):516-29.
48. Manicassamy S, Reizis B, Ravindran R, Nakaya H, Salazar-Gonzalez RM, Wang YC, Pulendran B. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science. 2010 Aug 13;329(5993):849-53.
49. Tang H, Cao W, Kasturi SP, Ravindran R, Nakaya HI, Kundu K, Murthy N, Kepler TB, Malissen B, Pulendran B. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nature Immunology. 2010 Jul;11(7):608-17.
50. de Mello Varani A, Souza RC, Nakaya HI, de Lima WC, Paula de Almeida LG, Kitajima EW, Chen J, Civerolo E, Vasconcelos AT, Van Sluys MA. Origins of the Xylellafastidiosa prophage-like regions and their impact in genome differentiation. PLoS One. 2008;3(12):e4059.
51. Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, Pirani A, Gernert K, Deng J, Marzolf B, Kennedy K, Wu H, Bennouna S, Oluoch H, Miller J, Vencio RZ, Mulligan M, Aderem A, Ahmed R, Pulendran B. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nature Immunology. 2009 Jan;10(1):116-25.
52. Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S. Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics. 2008 Jul;92(1):18-25.
53. Nakaya HI, Beckedorff FC, Baldini ML, Fachel AA, Reis EM, Verjovski-Almeida S. Splice variants of TLE family genes and up-regulation of a TLE3 isoform in prostate tumors. BiochemBiophys Res Commun. 2007 Dec 28;364(4):918-23.
54. Zaini PA, Fogaça AC, Lupo FG, Nakaya HI, Vêncio RZ, da Silva AM. The iron stimulon of Xylellafastidiosa includes genes for type IV pilus and colicin V-like bacteriocins. J Bacteriol. 2008 Apr;190(7):2368-78.
55. Nakaya HI, Amaral PP, Louro R, Lopes A, Fachel AA, Moreira YB, El-Jundi TA, da Silva AM, Reis EM, Verjovski-Almeida S. Genome mapping and expression analyses of human intronic noncoding RNAs reveal tissue-specific patterns and enrichment in genes related to regulation of transcription. Genome Biol. 2007;8(3):R43.
56. Louro R, Nakaya HI, Amaral PP, Festa F, Sogayar MC, da Silva AM, Verjovski-Almeida S, Reis EM. Androgenresponsiveintronic non-codingRNAs. BMC Biol. 2007 Jan 30;5:4.
57. Reis EM, Louro R, Nakaya HI, Verjovski-Almeida S. As antisense RNA getsintronic. OMICS. 2005 Spring;9(1):2-12.
58. Reis EM, Nakaya HI, Louro R, Canavez FC, Flatschart AV, Almeida GT, Egidio CM, Paquola AC, Machado AA, Festa F, Yamamoto D, Alvarenga R, da Silva CC, Brito GC, Simon SD, Moreira-Filho CA, Leite KR, Camara-Lopes LH, Campos FS, Gimba E, Vignal GM, El-Dorry H, Sogayar MC, Barcinski MA, da Silva AM, Verjovski-Almeida S. Antisenseintronic non-coding RNA levels correlate tothedegreeof tumor differentiation in prostatecancer. Oncogene. 2004 Aug 26;23(39):6684-92.
59. Louro R, Nakaya HI, Paquola AC, Martins EA, da Silva AM, Verjovski-Almeida S, Reis EM. RASL11A, member of a novel small monomeric GTPase gene family, is down-regulated in prostate tumors. BiochemBiophys Res Commun. 2004 Apr 9;316(3):618-27.

Book Chapters

1. Nakaya HI, Reis EM, Verjovski-Almeida S (2007) Concepts on microarray design for genome and transcriptome analyses. Chapter of book “Nucleic acid hybridization: modern applications”, Editors: Anton A. Buzdin e Sergey A. Lukyanov, Publisher: Springer.
2. Duraisingham SS, Rouphael N, Cavanagh MM, Nakaya HI, Goronzy JJ, Pulendran B. (2013) Systems biology of vaccination in the elderly. Curr Top Microbiol Immunol. 363:117-42.
3. Nakaya HI (2013) Applying Systems Biology to Understand the Immune Response to Infection and Vaccination. Chapter of book “Computational Systems Biology, 2nd Ed”, Editors: Elis &Kriete, Publisher: Elsevier