Strict tropism for CD71+/CD234+ human reticulocytes limits the zoonotic potential of Plasmodium cynomolgi

Kosaisavee, Varakorn; Suwanarusk, Rossarin; Chua, Adeline C. Y.; Kyle, Dennis E.; Malleret, Benoît; Zhang, Rou; Imwong, Mallika; Im-Erbsin, Rawiwan; Ubalee, Ratawan; Sámano-Sánchez, Hugo; Yeung, Bryan K. S.; Ong, Jessica Jie Ying; Lombardini, Eric; Nosten, François; Tan, Kevin S. W.; Bifani, Pablo; Snounou, Georges; Rénia, Laurent; Russell, Bruce

doi:10.1182/blood-2017-02-764787

Cited by 24 publications

(25 citation statements)

References 28 publications

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“…Only one case of a human naturally infected with P. cynomolgi has been reported, which was in Peninsular Malaysia [ 30 ], while no natural human infection by P. inui has been reported. Human infections by P. cynomolgi could be limited by its requirement for select receptors on human RBCs [ 45 ]. Lack of suitable vectors could also affect invasion of human RBCs by these species.…”

Section: Discussionmentioning

confidence: 99%

Absence of Plasmodium inui and Plasmodium cynomolgi, but detection of Plasmodium knowlesi and Plasmodium vivax infections in asymptomatic humans in the Betong division of Sarawak, Malaysian Borneo

Siner

Liew

Kadir

et al. 2017

Malar J

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Background Plasmodium knowlesi, a simian malaria parasite, has become the main cause of malaria in Sarawak, Malaysian Borneo. Epidemiological data on malaria for Sarawak has been derived solely from hospitalized patients, and more accurate epidemiological data on malaria is necessary. Therefore, a longitudinal study of communities affected by knowlesi malaria was undertaken.MethodsA total of 3002 blood samples on filter paper were collected from 555 inhabitants of 8 longhouses with recently reported knowlesi malaria cases in the Betong Division of Sarawak, Malaysian Borneo. Each longhouse was visited bimonthly for a total of 10 times during a 21-month study period (Jan 2014–Oct 2015). DNA extracted from blood spots were examined by a nested PCR assay for Plasmodium and positive samples were then examined by nested PCR assays for Plasmodium falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale, Plasmodium knowlesi, Plasmodium cynomolgi and Plasmodium inui. Blood films of samples positive by PCR were also examined by microscopy.ResultsGenus-specific PCR assay detected Plasmodium DNA in 9 out of 3002 samples. Species-specific PCR identified 7 P. knowlesi and one P. vivax. Malaria parasites were observed in 5 thick blood films of the PCR positive samples. No parasites were observed in blood films from one knowlesi-, one vivax- and the genus-positive samples. Only one of 7 P. knowlesi-infected individual was febrile and had sought medical treatment at Betong Hospital the day after sampling. The 6 knowlesi-, one vivax- and one Plasmodium-infected individuals were afebrile and did not seek any medical treatment.ConclusionsAsymptomatic human P. knowlesi and P. vivax malaria infections, but not P. cynomolgi and P. inui infections, are occurring within communities affected with malaria.

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Section: Discussionmentioning

confidence: 99%

Absence of Plasmodium inui and Plasmodium cynomolgi, but detection of Plasmodium knowlesi and Plasmodium vivax infections in asymptomatic humans in the Betong division of Sarawak, Malaysian Borneo

Siner

Liew

Kadir

et al. 2017

Malar J

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“…Plasmodium cynomolgi is a closely related zoonotic macaque parasite that has recently been isolated from human hosts [49]. Like P. knowlesi, P. cynomolgi invades macaque erythrocytes indiscriminately, but is reticulocyte-restricted in human blood, potentially limiting its zoonotic potential [50]. Kosaisavee et al .…”

Section: Monkey In the Middle: The Emerging Public Health Threat Posementioning

confidence: 99%

“…Kosaisavee et al . [50] revealed that this phenotype is attributable to the reliance of this parasite upon transferrin receptor 1 and the Duffy antigen/receptor for chemokines (DARC) during human erythrocyte invasion. Long-term in vitro culture of P. cynomolgi in human blood and comparison with P. knowlesi may reveal convergent mechanisms of adaptation to the human host and offer novel insight into process of zoonotic emergence.…”

Section: Monkey In the Middle: The Emerging Public Health Threat Posementioning

confidence: 99%

Molecular interactions governing host-specificity of blood stage malaria parasites

Scully

Kanjee

Duraisingh

2017

Current Opinion in Microbiology

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Non-human primates harbor diverse species of malaria parasites, including the progenitors of P. falciparum and P. vivax. Cross-species transmission of some malaria parasites—most notably the macaque parasite, P. knowlesi—continues to this day, compelling the scientific community to ask whether these zoonoses could impede malaria control efforts by acting as a source of recurrent human infection. Host-restriction varies considerably among parasite species and is governed by both ecological and molecular variables. In particular, the efficiency of red blood cell invasion constitutes a prominent barrier to zoonotic emergence. Although proteins expressed upon the erythrocyte surface exhibit considerable diversity both within and among hosts, malaria parasites have adapted to this heterogeneity via the expansion of protein families associated with invasion, offering redundant mechanisms of host cell entry. This molecular toolkit may enable some parasites to circumvent host barriers, potentially yielding host shifts upon subsequent adaptation. Recent studies have begun to elucidate the molecular determinants of host-specificity, as well as the mechanisms that malaria parasites use to overcome these restrictions. We review recent studies concerning host tropism in the context of erythrocyte invasion by focusing on three malaria parasites that span the zoonotic spectrum: P. falciparum, P. knowlesi, and P. vivax.

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“…On the basis of the results, the Fy b-long -expressing K562 erytholeukemia cell line was selected for differentiation and enucleation studies. Although permissivity for these P. vivax-type parasites may not be definitive proof that the cells are also P. vivax permissive, P. knowlesi and P. cynomolgi were chosen based on the fact that they are good models for the Fy receptor-dependent invasion of red cells [20,21], where P. cynomolgi, in particular, is the parasite phylogenetically and biologically most closely related to P. vivax.…”

Section: Discussionmentioning

confidence: 99%

“…It is well known that P. vivax [19] and its closely related non-human primate malarias P. knowlesi [20] and P. cynomolgi [21] require the Duffy blood group antigen receptor to invade their host red blood cells. However, the K562 erythroleukemia cell line does not express this antigen.…”

Section: Generation Of Fy Receptor-expressing K562 Cell Linesmentioning

confidence: 99%

K562 erythroleukemia line as a possible reticulocyte source to culture Plasmodium vivax and its surrogates

Kronstein‐Wiedemann

Klop

Thiel

et al. 2020

Experimental Hematology

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Establishing an in vitro "red blood cell matrix" that would allow uninterrupted access to a stable, homogeneous reticulocyte population would facilitate the establishment of continuous, long-term in vitro Plasmodium vivax blood stage cultures. In this study, we have explored the suitability of the erythroleukemia K562 cell line as a continuous source of such reticulocytes and have investigated regulatory factors behind the terminal differentiation (and enucleation, in particular) of this cell line that can be used to drive the reticulocyte production process. The Duffy blood group antigen receptor (Fy), essential for P. vivax invasion, was stably introduced into K562 cells by lentiviral gene transfer. miRNA-26a-5p and miRNA-30a-5p were downregulated to promote erythroid differentiation and enucleation, resulting in a tenfold increase in the production of reticulocytes after stimulation with an induction cocktail compared with controls. Our results suggest an interplay in the mechanisms of action of miRNA-26a-5p and miRNA-30a-5p, which makes it necessary to downregulate both miRNAs to achieve a stable enucleation rate and Fy receptor expression. In the context of establishing P. vivax-permissive, stable, and reproducible reticulocytes, a higher enucleation rate may be desirable, which may be achieved by the targeting of further regulatory mechanisms in Fy-K562 cells; promoting the shift in hemoglobin production from fetal to adult may also be necessary. Despite the fact that K562 erythroleukemia cell lines are of neoplastic origin, this cell line offers a versatile model system to research the regulatory mechanisms underlying erythropoiesis.

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Strict tropism for CD71+/CD234+ human reticulocytes limits the zoonotic potential of Plasmodium cynomolgi

Cited by 24 publications

References 28 publications

Absence of Plasmodium inui and Plasmodium cynomolgi, but detection of Plasmodium knowlesi and Plasmodium vivax infections in asymptomatic humans in the Betong division of Sarawak, Malaysian Borneo

Absence of Plasmodium inui and Plasmodium cynomolgi, but detection of Plasmodium knowlesi and Plasmodium vivax infections in asymptomatic humans in the Betong division of Sarawak, Malaysian Borneo

Molecular interactions governing host-specificity of blood stage malaria parasites

K562 erythroleukemia line as a possible reticulocyte source to culture Plasmodium vivax and its surrogates

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