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Developing Plasmodium vivax Resources for Liver Stage Study in the Peruvian Amazon Region

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    Developing Plasmodium vivax Resources for Liver Stage Study in the Peruvian Amazon Region
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    • Pamela Orjuela-Sanchez
      Pamela Orjuela-Sanchez
      Division of Host-Microbe Systems and Therapeutics, Health Sciences Center for Immunology, Infection and Inflammation, Department of Pediatrics, School of Medicine, University of California, San Diego, 9500 Gilman Drive #0760, La Jolla, California 92093-0760, United States
      More by Pamela Orjuela-Sanchez
      Orcidhttp://orcid.org/0000-0002-1093-9105
    • Zaira Hellen Villa
      Zaira Hellen Villa
      Laboratorio ICEMR-Amazonia, Laboratorios de Investigacion y Desarrollo, Facultad de Ciencias y Filosofia, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, San Martín de Porres, Lima, 15102, Peru
      More by Zaira Hellen Villa
    • Marta Moreno
      Marta Moreno
      Division of Infectious Diseases, Department of Medicine, University of California, San Diego, 9500 Gilman Drive #0760, La Jolla, California 92093-0760, United States
      More by Marta Moreno
    • Carlos Tong-Rios
      Carlos Tong-Rios
      Laboratorio ICEMR-Amazonia, Laboratorios de Investigacion y Desarrollo, Facultad de Ciencias y Filosofia, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, San Martín de Porres, Lima, 15102, Peru
      More by Carlos Tong-Rios
    • Stephan Meister
      Stephan Meister
      Division of Host-Microbe Systems and Therapeutics, Health Sciences Center for Immunology, Infection and Inflammation, Department of Pediatrics, School of Medicine, University of California, San Diego, 9500 Gilman Drive #0760, La Jolla, California 92093-0760, United States
      More by Stephan Meister
    • Gregory M. LaMonte
      Gregory M. LaMonte
      Division of Host-Microbe Systems and Therapeutics, Health Sciences Center for Immunology, Infection and Inflammation, Department of Pediatrics, School of Medicine, University of California, San Diego, 9500 Gilman Drive #0760, La Jolla, California 92093-0760, United States
      More by Gregory M. LaMonte
    • Brice Campo
      Brice Campo
      Medicines for Malaria Venture (MMV), International Center Cointrin, Block G, 20 Route de Pre-Bois, POB 1826, Geneva, CH-1215, Switzerland
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    • Joseph M. Vinetz
      Joseph M. Vinetz
      Laboratorio ICEMR-Amazonia, Laboratorios de Investigacion y Desarrollo, Facultad de Ciencias y Filosofia, Universidad Peruana Cayetano Heredia, Av. Honorio Delgado 430, San Martín de Porres, Lima, 15102, Peru
      Division of Infectious Diseases, Department of Medicine, University of California, San Diego, 9500 Gilman Drive #0760, La Jolla, California 92093-0760, United States
      Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, Lima, 15102, Peru
      More by Joseph M. Vinetz
      Orcidhttp://orcid.org/0000-0001-8344-2004
    • Elizabeth A. Winzeler*
      Elizabeth A. Winzeler
      Division of Host-Microbe Systems and Therapeutics, Health Sciences Center for Immunology, Infection and Inflammation, Department of Pediatrics, School of Medicine, University of California, San Diego, 9500 Gilman Drive #0760, La Jolla, California 92093-0760, United States
      *E-mail: [email protected]
      More by Elizabeth A. Winzeler
      Orcidhttp://orcid.org/0000-0002-4049-2113
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    ACS Infectious Diseases

    Cite this: ACS Infect. Dis. 2018, 4, 4, 531–540
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsinfecdis.7b00198
    Published March 15, 2018
    Copyright © 2018 American Chemical Society
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    Abstract

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    To develop new drugs and vaccines for malaria elimination, it will be necessary to discover biological interventions, including small molecules that act against Plasmodium vivax exoerythrocytic forms. However, a robust in vitro culture system for P. vivax is still lacking. Thus, to study exoerythrocytic forms, researchers must have simultaneous access to fresh, temperature-controlled patient blood samples, as well as an anopheline mosquito colony. In addition, researchers must rely on native mosquito species to avoid introducing a potentially dangerous invasive species into a malaria-endemic region. Here, we report an in vitro culture system carried out on site in a malaria-endemic region for liver stage parasites of P. vivax sporozoites obtained from An. darlingi, the main malaria vector in the Americas. P. vivax sporozoites were obtained by dissection of salivary glands from infected An. darlingi mosquitoes and purified by Accudenz density gradient centrifugation. HC04 liver cells were exposed to P. vivax sporozoites and cultured up to 9 days. To overcome low P. vivax patient parasitemias, potentially lower mosquito vectorial capacity, and humid, nonsterile environmental conditions, a new antibiotic cocktail was included in tissue culture to prevent contamination. Culturing conditions supported exoerythrocytic (EEF) P. vivax liver stage growth up to 9 days and allowed for maturation into intrahepatocyte merosomes. Some of the identified small forms were resistant to atovaquone (1 μM) but sensitive to the phosphatidylinositol 4-kinase inhibitor, KDU691 (1 μM). This study reports a field-accessible EEF production process for drug discovery in a malaria-endemic site in which viable P. vivax sporozoites are used for drug studies using hepatocyte infection. Our data demonstrate that the development of meaningful, field-based resources for P. vivax liver stage drug screening and liver stage human malaria experimentation in the Amazon region is feasible.

    Copyright © 2018 American Chemical Society

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    Cited By

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    This article is cited by 8 publications.

    1. Marta Moreno, Carlos Tong-Rios, Pamela Orjuela-Sanchez, Gabriel Carrasco-Escobar, Brice Campo, Dionicia Gamboa, Elizabeth A. Winzeler, Joseph M. Vinetz. Continuous Supply of Plasmodium vivax Sporozoites from Colonized Anopheles darlingi in the Peruvian Amazon. ACS Infectious Diseases 2018, 4 (4) , 541-548. https://doi.org/10.1021/acsinfecdis.7b00195
    2. Alice O. Andrade, Najara Akira C. Santos, Alessandra S. Bastos, José Daniel C. Pontual, Cristiane S. Araújo, Analice S. Lima, Leandro N. Martinez, Amália S. Ferreira, Anna Caroline C. Aguiar, Carolina B. G. Teles, Rafael V. C. Guido, Rosa A. Santana, Stefanie C. P. Lopes, Jansen F. Medeiros, Zaira Rizopoulos, Joseph M. Vinetz, Brice Campo, Marcus Vinicius G. Lacerda, Maisa S. Araújo. Optimization of Plasmodium vivax infection of colonized Amazonian Anopheles darlingi. Scientific Reports 2023, 13 (1) https://doi.org/10.1038/s41598-023-44556-y
    3. Katherine Torres, Marcelo U. Ferreira, Marcia C. Castro, Ananias A. Escalante, Jan E. Conn, Elizabeth Villasis, Maisa da Silva Araujo, Gregorio Almeida, Priscila T. Rodrigues, Rodrigo M. Corder, Anderson R. J. Fernandes, Priscila R. Calil, Winni A. Ladeia, Stefano S. Garcia-Castillo, Joaquin Gomez, Lis Ribeiro do Valle Antonelli, Ricardo T. Gazzinelli, Douglas T. Golenbock, Alejandro Llanos-Cuentas, Dionicia Gamboa, Joseph M. Vinetz. Malaria Resilience in South America: Epidemiology, Vector Biology, and Immunology Insights from the Amazonian International Center of Excellence in Malaria Research Network in Peru and Brazil. The American Journal of Tropical Medicine and Hygiene 2022, 107 (4_Suppl) , 168-181. https://doi.org/10.4269/ajtmh.22-0127
    4. Euzebiusz Jamrozik, Michael J. Selgelid. Ethical Issues. 2021, 25-82. https://doi.org/10.1007/978-3-030-41480-1_3
    5. Pradeep A. Subramani, Neha Vartak-Sharma, Seetha Sreekumar, Pallavi Mathur, Bhavana Nayer, Sushrut Dakhore, Sowmya K. Basavanna, Devaiah M. Kalappa, Ramya V. Krishnamurthy, Benudhar Mukhi, Priyasha Mishra, Noriko Yoshida, Susanta Kumar Ghosh, Radhakrishan Shandil, Shridhar Narayanan, Brice Campo, Kouichi Hasegawa, Anupkumar R. Anvikar, Neena Valecha, Varadharajan Sundaramurthy. Plasmodium vivax liver stage assay platforms using Indian clinical isolates. Malaria Journal 2020, 19 (1) https://doi.org/10.1186/s12936-020-03284-8
    6. Dora Posfai, Steven P. Maher, Camille Roesch, Amélie Vantaux, Kayla Sylvester, Julie Péneau, Jean Popovici, Dennis E. Kyle, Benoît Witkowski, Emily R. Derbyshire. Plasmodium vivax Liver and Blood Stages Recruit the Druggable Host Membrane Channel Aquaporin-3. Cell Chemical Biology 2020, 27 (6) , 719-727.e5. https://doi.org/10.1016/j.chembiol.2020.03.009
    7. Melanie J. Shears, Sean C. Murphy. Vancomycin improves Plasmodium yoelii malaria parasite in vitro liver stage cultures by controlling Elizabethkingia anophelis, a bacterium in the microbiome of lab-reared Anopheles mosquitoes. Molecular and Biochemical Parasitology 2020, 237 , 111279. https://doi.org/10.1016/j.molbiopara.2020.111279
    8. Gregory M. LaMonte, Pamela Orjuela-Sanchez, Jaeson Calla, Lawrence T. Wang, Shangzhong Li, Justine Swann, Annie N. Cowell, Bing Yu Zou, Alyaa M. Abdel-Haleem Mohamed, Zaira Hellen Villa Galarce, Marta Moreno, Carlos Tong Rios, Joseph M. Vinetz, Nathan Lewis, Elizabeth A. Winzeler. Dual RNA-seq identifies human mucosal immunity protein Mucin-13 as a hallmark of Plasmodium exoerythrocytic infection. Nature Communications 2019, 10 (1) https://doi.org/10.1038/s41467-019-08349-0
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    ACS Infectious Diseases

    Cite this: ACS Infect. Dis. 2018, 4, 4, 531–540
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsinfecdis.7b00198
    Published March 15, 2018
    Copyright © 2018 American Chemical Society
    Request reuse permissions

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