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  1. Science & Research (Biologics)

Improving the Safety of Blood and Blood Related Products by Reducing the Risk of Transfusion-Transmission of Leishmania Parasites

Hira Nakhasi, PhD., FASTMH

Office of Blood Research and Review
Division of Emerging and Transfusion Transmitted Diseases
Laboratory of Emerging Pathogens

Hira.Nakhasi@fda.hhs.gov

Biosketch

I am the Director of the Division of Emerging and Transfusion Transmitted Diseases in the Office of Blood Research and Review (OBRR) at the Center for Biologics Evaluation and Research (CBER) of FDA.  I received my Masters and Ph.D. in biochemistry from the M.S. University in Baroda, India and post-doctoral training at the National Institutes of Health in Bethesda, MD, USA and Columbia University in NY.   Before my current position, I was also the acting associate director for Research in OBRR/CBER and Chief of Laboratory of Parasitic Biology and Biochemistry in the Division of Allergenic and Parasitic Products, in the Office of Vaccines Research and Review at CBER.

My main research focus is on the development of Leishmania donovani vaccine and diagnosis. My laboratory is also developing diagnostic reagents for blood-borne parasitic pathogens to ensure the safety of our nation’s blood supply.

My scientific expertise in molecular virology, parasitology, immunology and vaccinology is reflected in over 130 publications, including reviews and book chapters and membership of the review committees of several high impact journals, reviewer of grants, and invited talks at national and international forums. My research on Leishmania vaccine is partially funded by research grants from various sources.  I am also a member of several scientific organizations, including the American Association of Immunologists, American Society of Microbiologists, American Society of Tropical Medicine and Hygiene, and a Fellow of the American Society of Tropical Medicine and Hygiene (FASTMH). I have also received numerous awards, including the US Department of Human and Health Services Distinguished Service Award.

General Overview

Leishmaniasis is a vector-borne disease caused by Leishmania parasites transmitted by the bite of certain species of sand fly in parts of South America, Africa, Southeast Asia, the Middle East, and Southern and Eastern Europe. It has been designated by the World Health Organization as one of the top 10 neglected tropical diseases. Environmental changes such as global warming or human migrations have affected the vector-reservoir-host triad and led an expansion of the leishmaniasis geographical range. Co-infection of HIV and visceral leishmaniasis has led to the reemergence of visceral leishmaniasis in Leishmania non-endemic countries.

United States military personnel or civilians stationed in areas of the world where leishmaniasis occurs are at risk of infection. This threat has increased in recent years because of extensive travel to these areas by US citizens and migration of people from endemic areas. Recently, it has been reported that local cases of Leishmania infection are occurring in the southern states of US.

Depending on the specific type of the disease, a person with leishmaniasis can develop disfiguring ulcers in the skin, nose, mouth, or throat; or suffer potentially fatal spleen or liver damage. Transfusions of blood from infected donors can also spread the parasite.

Approximately 12 million people are infected worldwide, > 350 million people at risk, with more than half a million new clinical cases reported annually and ~50,000 deaths annually. There are no vaccines or donor screening assays for Leishmania parasites. In addition, immigration from Latin American, Asian, African and Middle Eastern countries where incidence of Leishmaniasis is increasing because of the failure of health care system, non-compliance to drug treatment and political unrest in some of these countries poses a serious risk of spread of the disease in the US. 90% of human visceral leishmaniasis infections are asymptomatic and can transmit Leishmania parasite through blood transfusion. Industry is currently developing vaccines and diagnostic tests for Leishmania infection for evaluation by FDA.

One of the major obstacles to detecting the parasites in blood is that they occur in very low numbers. Therefore, we are developing methods using state-of-art technologies to solve that problem.

My laboratory is evaluating the safety and efficacy of various vaccine candidates, including genetically modified live attenuated parasites. We are also developing biomarkers of safety and immunity that can be used by the manufacturers to test the safety and effectiveness of such vaccines before submitting them to FDA for evaluation.

Scientific Overview

In addition, we have developed genetically modified Leishmania donovani parasites and performing preclinical evaluation of their immunogenicity and safety in animal models, such as mice, hamsters and dogs. We also are evaluating their immunogenicity in peripheral blood mononuclear cells form normal and infected individuals from the endemic regions of Leishmania.

Following are the specific regulatory challenges that my laboratory is trying to address regarding Leishmania vaccines.

  1. What are the differences in immune and non-immune biomarkers of immunogenicity among various Leishmania vaccine candidates (recombinant vs. genetically modified vaccines) and can some of the biomarkers predict protection in the clinical setting?
  2. Will Leishmania vaccines protect both lethal and non-lethal Leishmania infections?
  3. Will Leishmania vaccines protect in the presence of other co-parasitic infections, such as malaria and Chagas, which are common in the Leishmania endemic regions?
  4. Approximately 90% of the individuals who are infected with Leishmania do not show any symptoms. These individuals can transmit infections to non-infected individuals, either through blood transfusion or through the sand fly vector. Therefore, will Leishmania vaccine be effective in asymptomatic individuals?
  5. Natural infection in endemic areas occurs through the bite of an infected sand fly, which is the vector for Leishmania. Can Leishmania vaccines be effective against infection via sand fly bite in preclinical studies? 

To address the above-mentioned questions, we have accomplished some of the goals and are pursuing the others. These studies are being conducted in collaboration with scientists from with National Institute of Allergy and Infectious Diseases (NIH), Ohio State University, McGill University (Montreal, Canada) and the Institute of Tropical Medicine (Nagasaki University, Japan).

Publications

  1. ACS Infect Dis 2024 Aug 7 [Epub ahead of print]
    Identifying Rab2 protein as a key interactor of Centrin1 essential for Leishmania donovani growth.
    Roshanara, Tandon R, Baig MS, Das S, Srivastava R, Puri N, Nakhasi HL, Selvapandiyan A
  2. Microbes Infect 2024 Jul-Aug;26(5-6):105340
    Proteome profile of Leishmania donovani Centrin1(-/-) parasite-infected human macrophage cell line and its implications in determining possible mechanisms of protective immunity.
    Reyaz E, Tandon R, Beg MA, Dey R, Puri N, Salotra P, Nakhasi HL, Selvapandiyan A
  3. Sci Rep 2024 Jun 25;14(1):14636
    Manufacturing and preclinical toxicity of GLP grade gene deleted attenuated Leishmania donovani parasite vaccine.
    Avishek K, Beg MA, Vats K, Singh AK, Dey R, Singh KP, Singh RK, Gannavaram S, Ramesh V, Mulla MSA, Bhatnagar U, Singh S, Nakhasi HL, Salotra P, Selvapandiyan A
  4. Vaccines 2024 Mar 15;12(3):310
    Immunization with centrin-deficient Leishmania braziliensis does not protect against homologous challenge.
    Avendano-Rangel F, Agra-Duarte G, Borba PB, Moitinho V, Avila LT, da Silva LO, Viana SM, Sharma R, Gannavaram S, Nakhasi HL, de Oliveira CI
  5. Microorganisms 2024 Jan 29;12(2):280
    The preclinical validation of 405 nm light parasiticidal efficacy on Leishmania donovani in ex vivo platelets in a Rag2(-/-) mouse model.
    Kaldhone PR, Azodi N, Markle HL, Dahiya N, Stewart C, Anderson J, MacGregor S, Maclean M, Nakhasi HL, Gannavaram S, Atreya C
  6. iScience 2023 Dec 15;26(12):108502
    Leishmania mexicana promotes pain-reducing metabolomic reprogramming in cutaneous lesions.
    Volpedo G, Oljuskin T, Cox B, Mercado Y, Askwith C, Azodi N, Bernier M, Nakhasi HL, Gannavaram S, Satoskar AR
  7. Nat Commun 2023 Nov 2;14(1):7028
    Production of leishmanin skin test antigen from Leishmania donovani for future reintroduction in the field.
    Dey R, Alshaweesh J, Singh KP, Lypaczewski P, Karmakar S, Klenow L, Paulini K, Kaviraj S, Kamhawi S, Valenzuela JG, Singh S, Hamano S, Satoskar AR, Gannavaram S, Nakhasi HL, Matlashewski G
  8. Cell Rep 2023 Sep 26;42(9):113097
    Dual-scRNA-seq analysis reveals rare and uncommon parasitized cell populations in chronic L. donovani infection.
    Karagiannis K, Gannavaram S, Verma C, Pacheco-Fernandez T, Bhattacharya P, Nakhasi HL, Satoskar AR
  9. iScience 2023 Sep 15;26(9):107594
    Leishmania mexicana centrin knockout parasites promote M1-polarizing metabolic changes.
    Volpedo G, Pacheco-Fernandez T, Oljuskin T, Markle HL, Azodi N, Hamano S, Matlashewski G, Gannavaram S, Nakhasi HL, Satoskar AR
  10. iScience 2023 Sep 15;26(9):107593
    Leishmania major centrin knock-out parasites reprogram tryptophan metabolism to induce a pro-inflammatory response.
    Oljuskin T, Azodi N, Volpedo G, Bhattacharya P, Markle HL, Hamano S, Matlashewski G, Satoskar AR, Gannavaram S, Nakhasi HL
  11. Res Rep Trop Med 2023 Jul 20;14:61-85
    Field-deployable treatments for leishmaniasis: intrinsic challenges, recent developments and next steps.
    Pacheco-Fernandez T, Markle H, Verma C, Huston R, Gannavaram S, Nakhasi HL, Satoskar AR
  12. Sci Rep 2023 May 5;13(1):7362
    Deletion of MIF gene from live attenuated LdCen(-/-) parasites enhances protective CD4(+) T cell immunity.
    Fiuza JA, Gannavaram S, Gaze ST, de Ornellas LG, Alves ÉA, Ismail N, Nakhasi HL, Correa-Oliveira R
  13. Pathogens 2023 Mar 29;12(4):534
    Toll-like receptor-9 (TLR-9) signaling is crucial for inducing protective immunity following immunization with genetically modified live attenuated Leishmania parasites.
    Bhattacharya P, Gannavaram S, Ismail N, Saxena A, Dagur PK, Akue A, KuKuruga M, Nakhasi HL
  14. Parasitol Int 2023 Feb;92:102661
    Identification of protein biomarkers of attenuation and immunogenicity of centrin or p27 gene deleted live vaccine candidates of Leishmania against visceral leishmaniasis.
    Tandon R, Reyaz E, Roshanara, Jadhav M, Gandhi M, Dey R, Salotra P, Nakhasi HL, Selvapandiyan A
  15. NPJ Vaccines 2022 Dec 3;7(1):157
    Centrin-deficient Leishmania mexicana confers protection against Old World visceral leishmaniasis.
    Karmakar S, Volpedo G, Zhang WW, Lypaczewski P, Ismail N, Oliveira F, Oristian J, Meneses C, Gannavaram S, Kamhawi S, Hamano S, Valenzuela JG, Matlashewski G, Satoskar AR, Dey R, Nakhasi HL
  16. Pathogens 2022 Apr 2;11(4):431
    The history of live attenuated centrin gene-deleted Leishmania vaccine candidates.
    Volpedo G, Bhattacharya P, Gannavaram S, Pacheco-Fernandez T, Oljuskin T, Dey R, Satoskar AR, Nakhasi HL
  17. Front Immunol 2022 Mar 28;13:864031
    Leishmania major centrin gene-deleted parasites generate skin resident memory T-cell immune response analogous to leishmanization.
    Ismail N, Karmakar S, Bhattacharya P, Sepahpour T, Takeda K, Hamano S, Matlashewski G, Satoskar AR, Gannavaram S, Dey R, Nakhasi HL
  18. NPJ Vaccines 2022 Mar 2;7(1):32
    Centrin-deficient Leishmania mexicana confers protection against New World cutaneous leishmaniasis.
    Volpedo G, Pacheco-Fernandez T, Holcomb EA, Zhang WW, Lypaczewski P, Cox B, Fultz R, Mishan C, Verma C, Huston RH, Wharton AR, Dey R, Karmakar S, Oghumu S, Hamano S, Gannavaram S, Nakhasi HL, Matlashewski G, Satoskar AR
  19. PLoS Negl Trop Dis 2022 Feb 22;16(2):e0010224
    Neutrophil-dendritic cell interaction plays an important role in live attenuated Leishmania vaccine induced immunity.
    Bhattacharya P, Ismail N, Saxena A, Gannavaram S, Dey R, Oljuskin T, Akue A, Takeda K, Yu J, Karmakar S, Dagur PK, McCoy JP Jr, Nakhasi HL
  20. Expert Rev Vaccines 2021 Nov;20(11):1431-46
    From infection to vaccination: reviewing the global burden, history of vaccine development, and recurring challenges in global leishmaniasis protection.
    Volpedo G, Huston RH, Holcomb EA, Pacheco-Fernandez T, Gannavaram S, Bhattacharya P, Nakhasi HL, Satoskar AR
  21. Trends Parasitol 2021 Nov;37(11):976-87
    Leishmaniasis: the act of transmission.
    Serafim TD, Coutinho-Abreu IV, Dey R, Kissinger R, Valenzuela JG, Oliveira F, Kamhawi S
  22. Front Immunol 2021 Oct 12;12:748325
    Determinants of innate immunity in visceral leishmaniasis and their implication in vaccine development.
    Volpedo G, Pacheco-Fernandez T, Bhattacharya P, Oljuskin T, Dey R, Gannavaram S, Satoskar AR, Nakhasi HL
  23. J Immunol 2021 Sep 1;207(5):1322-32
    MicroRNA-21 deficiency promotes the early Th1 immune response and resistance toward visceral leishmaniasis.
    Varikuti S, Verma C, Holcomb E, Jha BK, Viana A, Maryala R, Lamenza F, McElwain BK, Doni NY, Papenfuss T, Oghumu S, Gannavaram S, Nakhasi HL, Satoskar AR
  24. Commun Biol 2021 Jul 30;4(1):929
    Preclinical validation of a live attenuated dermotropic Leishmania vaccine against vector transmitted fatal visceral leishmaniasis.
    Karmakar S, Ismail N, Oliveira F, Oristian J, Zhang WW, Kaviraj S, Singh KP, Mondal A, Das S, Pandey K, Bhattacharya P, Volpedo G, Gannavaram S, Satoskar M, Satoskar S, Sastry RM, Oljuskin T, Sepahpour T, Meneses C, Hamano S, Das P, Matlashewski G, Singh S, Kamhawi S, Dey R, Valenzuela JG, Satoskar A, Nakhasi HL
  25. Front Cell Infect Microbiol 2021 Mar 17;11:639801
    Revival of leishmanization and leishmanin.
    Pacheco-Fernandez T, Volpedo G, Gannavaram S, Bhattacharya P, Dey R, Satoskar A, Matlashewski G, Nakhasi HL
  26. J Immunol 2020 Dec 15;205(12):3333-47
    Essential role of neutrophils in the protective immune response induced by a live attenuated leishmania vaccine.
    Bhattacharya P, Dey R, Saxena A, Karmakar S, Ismail N, Gannavaram S, Dagur PK, Satoskar M, Satoskar S, De Paoli S, Takeda K, McCoy JP Jr, Nakhasi HL
  27. Cell Rep 2020 Oct 27;33(4):108317
    Heme oxygenase-1 induction by blood-feeding arthropods controls skin inflammation and promotes disease tolerance.
    DeSouza-Vieira T, Iniguez E, Serafim TD, de Castro W, Karmakar S, Disotuar MM, Cecilio P, Lacsina JR, Meneses C, Nagata BM, Cardoso S, Sonenshine DE, Moore IN, Borges VM, Dey R, Soares MP, Nakhasi HL, Oliveira F, Valenzuela JG, Kamhawi S
  28. Nat Commun 2020 Jul 10;11(1):3461
    A second generation leishmanization vaccine with a markerless attenuated Leishmania major strain using CRISPR gene editing.
    Zhang WW, Karmakar S, Gannavaram S, Dey R, Lypaczewski P, Ismail N, Siddiqui A, Simonyan V, Oliveira F, Coutinho-Abreu IV, DeSouza-Vieira T, Meneses C, Oristian J, Serafim TD, Musa A, Nakamura R, Saljoughian N, Volpedo G, Satoskar M, Satoskar S, Dagur PK, McCoy JP, Kamhawi S, Valenzuela JG, Hamano S, Satoskar AR, Matlashewski G, Nakhasi HL
  29. PLoS Negl Trop Dis 2019 Nov 18;13(11):e0007865
    Lymphocytes influence Leishmania major pathogenesis in a strain-dependent manner.
    Musa MA, Nakamura R, Hena A, Varikuti S, Nakhasi HL, Goto Y, Satoskar AR, Hamano S
  30. PLoS Negl Trop Dis 2019 Sep 19;13(9):e0007616
    Innovations for the elimination and control of visceral leishmaniasis.
    Selvapandiyan A, Croft SL, Rijal S, Nakhasi HL, Ganguly NK
  31. Front Immunol 2019 Sep 24;10:2273
    miR-21 expression determines the early vaccine immunity induced by LdCen(-/-) immunization.
    Gannavaram S, Bhattacharya P, Siddiqui A, Ismail N, Madhavan S, Nakhasi HL
  32. Vox Sang 2019 Jan;114(1):17-27
    International survey on the impact of parasitic infections: frequency of transmission and current mitigation strategies.
    Leiby DA, O'Brien SF, Wendel S, Nguyen ML, Delage G, Devare SG, Hardiman A, Nakhasi HL, Sauleda S, Bloch EM
  33. Front Immunol 2018 Nov 26;9:2741
    Leptin functions in infectious diseases.
    Maurya R, Bhattacharya P, Dey R, Nakhasi HL
  34. Parasitol Res 2018 Oct;117(10):3215-28
    A Leishmania-specific gene upregulated at the amastigote stage is crucial for parasite survival.
    Avishek K, Ahuja K, Pradhan D, Gannavaram S, Selvapandiyan A, Nakhasi HL, Salotra P
  35. Biochim Biophys Acta 2018 Aug;1865(8):1148-59
    A novel signal sequence negative multimeric glycosomal protein required for cell cycle progression of Leishmania donovani parasites.
    Ahuja K, Beg MA, Sharma R, Saxena A, Naqvi N, Puri N, Rai PK, Chaudhury A, Duncan R, Salotra P, Nakhasi H, Selvapandiyan A
  36. Front Immunol 2018 Jun 4;9:1176
    Centrin-deleted Leishmania donovani parasites help CD4+ T cells to acquire Th1 phenotype and multi-functionality through downregulation of CD200-CD200R immune inhibitory axis.
    Singh RK, Gannavaram S, Ismail N, Kaul A, Gedda MR, Nakhasi HL
  37. Parasitology 2018 Apr;145(4):443-52
    Dermotropic Leishmania donovani in Sri Lanka: visceralizing potential in clinical and preclinical studies.
    Kariyawasam KKGDUL, Selvapandiyan A, Siriwardana HVYD, Dube A, Karunanayake P, Senanayake SASC, Dey R, Gannavaram S, Nakhasi HL, Karunaweera ND
  38. Front Immunol 2017 Dec;8:1788
    Immunization with live attenuated Leishmania donovani Centrin(-/-) parasites is efficacious in asymptomatic infection.
    Ismail N, Kaul A, Bhattacharya P, Gannavaram S, Nakhasi HL
  39. Cell Host Microbe 2018 Jan 10;23(1):134-43
    Gut microbes egested during bites of infected sand flies augment severity of leishmaniasis via inflammasome-derived IL-1beta.
    Dey R, Joshi AB, Oliveira F, Pereira L, Guimarães-Costa AB, Serafim TD, de Castro W, Coutinho-Abreu IV, Bhattacharya P, Townsend S, Aslan H, Perkins A, Karmakar S, Ismail N, Karetnick M, Meneses C, Duncan R, Nakhasi HL, Valenzuela JG, Kamhawi S
  40. J Immunol 2018 Jan 1;200(1):163-76
    Live attenuated Leishmania donovani centrin gene-deleted parasites induce IL-23-dependent IL-17-protective immune response against visceral leishmaniasis in a murine model.
    Banerjee A, Bhattacharya P, Dagur PK, Karmakar S, Ismail N, Joshi AB, Akue AD, KuKuruga M, McCoy JP Jr, Dey R, Nakhasi HL
  41. BMC Infect Dis 2017 Dec 22;17(1):791
    Genetic diversity of Leishmania donovani that causes cutaneous leishmaniasis in Sri Lanka: a cross sectional study with regional comparisons.
    Kariyawasam UL, Selvapandiyan A, Rai K, Wani TH, Ahuja K, Beg MA, Premathilake HU, Bhattarai NR, Siriwardena YD, Zhong D, Zhou G, Rijal S, Nakhasi H, Karunaweera ND
  42. Sci Rep 2017 Oct 16;7(1):13240
    Role of mast cells in clearance of Leishmania through extracellular trap formation.
    Naqvi N, Ahuja K, Selvapandiyan A, Dey R, Nakhasi H, Puri N
  43. Sci Rep 2017 Oct 31;7(1):14693
    Ly6Chi inflammatory monocytes promote susceptibility to Leishmania donovani infection.
    Terrazas C, Varikuti S, Oghumu S, Steinkamp HM, Ardic N, Kimble J, Nakhasi H, Satoskar AR
  44. Sci Rep 2017 Jul 5;7(1):4718
    Whole genome sequencing of live attenuated Leishmania donovani parasites reveals novel biomarkers of attenuation and enables product characterization.
    Gannavaram S, Torcivia J, Gasparyan L, Kaul A, Ismail N, Simonyan V, Nakhasi HL
  45. Cell Immunol 2016 Nov;309:37-41
    Role of pro-inflammatory cytokine IL-17 in Leishmania pathogenesis and in protective immunity by Leishmania vaccines.
    Banerjee A, Bhattacharya P, Joshi AB, Ismail N, Dey R, Nakhasi HL
  46. Sci Rep 2016 Sep 14;6:33059
    Gene deleted live attenuated Leishmania vaccine candidates against visceral leishmaniasis elicit pro-inflammatory cytokines response in human PBMCs.
    Avishek K, Kaushal H, Gannavaram S, Dey R, Selvapandiyan A, Ramesh V, Negi NS, Dubey US, Nakhasi HL, Salotra P
  47. PLoS Negl Trop Dis 2016 Aug 31;10(8):e0004963
    Live attenuated Leishmania donovani centrin knock out parasites generate non-inferior protective immune response in aged mice against visceral leishmaniasis.
    Bhattacharya P, Dey R, Dagur PK, Joshi AB, Ismail N, Gannavaram S, Debrabant A, Akue AD, KuKuruga MA, Selvapandiyan A, McCoy JP Jr, Nakhasi HL
  48. Am J Trop Med Hyg 2016 Jul 6;95(1):109-19
    Differential Role of Leptin as an Immunomodulator in Controlling Visceral Leishmaniasis in Normal and Leptin-Deficient Mice.
    Maurya R, Bhattacharya P, Ismail N, Dagur PK, Joshi AB, Razdan K, McCoy JP Jr, Jill A, Dey R, Nakhasi HL
  49. Transfusion 2016 Jun;56(6 Pt 2):1537-47
    Multiplex detection and identification of viral, bacterial, and protozoan pathogens in human blood and plasma using a high-density resequencing pathogen microarray platform.
    Kourout M, Fisher C, Purkayastha A, Tibbetts C, Winkelman V, Williamson P, Nakhasi HL, Duncan R
  50. Front Immunol 2016 May 13;7:187
    Modulation of innate immune mechanisms to enhance Leishmania vaccine-induced immunity: role of coinhibitory molecules.
    Gannavaram S, Bhattacharya P, Ismail N, Kaul A, Singh R, Nakhasi HL
  51. J Appl Microbiol 2016 Apr;120(4):1119-29
    Standardized methods to generate mock (spiked) clinical specimens by spiking blood or plasma with cultured pathogens.
    Dong M, Fisher C, Anez G, Rios M, Nakhasi HL, Hobson JP, Beanan M, Hockman D, Grigorenko E, Duncan R
  52. Parasit Vectors 2016 Apr 30;9(1):250
    Application of rapid in vitro co-culture system of macrophages and T-cell subsets to assess the immunogenicity of dogs vaccinated with live attenuated Leishmania donovani centrin deleted parasites (LdCen-/-).
    Viana KF, Fiuza JA, Gannavaram S, Dey R, Selvapandiyan A, Bartholomeu DC, Silveira-Lemos DD, Bueno LL, Dutra WO, Fujiwara RT, Nakhasi HL, Giunchetti RC
  53. Methods Mol Biol 2016;1403:623-38
    Methods to evaluate the preclinical safety and immunogenicity of genetically modified live-attenuated Leishmania parasite vaccines.
    Gannavaram S, Bhattacharya P, Dey R, Ismail N, Avishek K, Salotra P, Selvapandiyan A, Satoskar A, Nakhasi HL
  54. PLoS Negl Trop Dis 2016 Jan 11;10(1):e0004322
    Intradermal immunization of Leishmania donovani centrin knock-out parasites in combination with salivary protein LJM19 from sand fly vector induces a durable protective immune response in hamsters.
    Fiuza JA, Dey R, Davenport D, Abdeladhim M, Meneses C, Oliveira F, Kamhawi S, Valenzuela JG, Gannavaram S, Nakhasi HL
  55. Infect Immun 2015 Oct;83(10):3800-15
    Genetically modified live attenuated L.donovani parasites induce innate immunity through classical activation of macrophages that direct Th1 response in mice.
    Bhattacharya P, Dey R, Dagur PK, Kruhlak M, Ismail N, Debrabant A, Joshi AB, Akue A, Kukuruga M, Takeda K, Selvapandiyan A, McCoy JP Jr, Nakhasi HL
  56. Proc Natl Acad Sci U S A 2015 Jul 28;112(30):E4094-103
    TACI deficiency leads to alternatively activated macrophage phenotype and susceptibility to Leishmania infection.
    Allman WR, Dey R, Liu L, Siddiqui S, Coleman AS, Bhattacharya P, Yano M, Uslu K, Takeda K, Nakhasi HL, Akkoyunlu M
  57. Vaccine 2015 Jan 3;33(2):280-8
    Vaccination using live attenuated Leishmania donovani centrin deleted parasites induces protection in dogs against Leishmania infantum.
    Fiuza JA, Gannavaram S, Santiago HD, Selvapandiyan A, Souza DM, Passos LS, Mendonca LZ, Lemos-Giunchetti DD, Ricci ND, Bartholomeu DC, Giunchetti RC, Bueno LL, Correa-Oliveira R, Nakhasi HL, Fujiwara RT
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