TOWARDS SUCCESSFUL ADAPTATION OF PLASMODIUM KNOWLESI TO LONG-TERM IN-VITRO CULTURE IN HUMAN ERYTHROCYTESHTML Full Text
TOWARDS SUCCESSFUL ADAPTATION OF PLASMODIUM KNOWLESI TO LONG-TERM IN-VITRO CULTURE IN HUMAN ERYTHROCYTES
F. S. Mohamad and N. Abu-Bakar *
School of Health Sciences, Health Campus, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan, Malaysia.
ABSTRACT: Plasmodium knowlesi, a simian malaria parasite, is widely used as a malaria model and now characterized as a clinically significant parasite that can lead to outbreaks throughout most countries in Southeast Asia. Despite its importance, both fundamental and clinical studies of P. knowlesi have been impeded by the lack of a convenient in-vitro culture system partly due to the parasite’s preference for reticulocytes. Due to a limited number of reticulocytes that could be collected from fresh sources such as umbilical cord, bone marrow, and peripheral blood, scientists have opted reticulocytes generated from CD34+ hematopoietic stem cells (HSCs) that have been cultured in an in-vitro system. With sufficient growth factors (GFs) and differentiation factors (DFs), a higher number and more homogenous populations of reticulocytes could be obtained from HSCs in-vitro. Here, we review an approach to produce massive expansion of CD34+ HSCs and their differentiation into reticulocytes that could be used for the establishment of a continuous in-vitro culture of P. knowlesi or P. vivax. The successful development of the long-term in-vitro culture of this parasite could ultimately provide an ideal system for forwarding diagnostic, anti-malarial drug and vaccine studies in malaria.
Plasmodium knowlesi, CD34+ hematopoietic stem cells, Reticulocytes, Erythrocytes, Parasite invasion
INTRODUCTION: Despite years of tremendous elimination efforts and progress, malaria remains as one of the most significant life-threatening diseases affecting people in tropical and subtropical regions. The World Malaria report 2017 reported that about 3.2 billion people were at risk of malaria, which accounts for nearly half of the world’s population. In 2016 alone, there were roughly 216 million malaria cases, an increase of 5 million cases over the previous year, an estimated 445,000 malaria deaths 1.
In the same year, Malaysia reported 2,327 malaria cases, which occurred mostly in Malaysian Borneo; Sabah and Sarawak, as well as in other states in Peninsular Malaysia such as Kelantan, Perak and Selangor 2.
Malaria is caused by hemoprotozoa from Plasmodium species and spread to humans through the bites of infected female Anopheles mosquitoes. P. falciparum is the most prevalent malaria parasite in sub-Saharan Africa, but outside of Africa, P. vivax is the predominant parasite in the region of the Americas, the Eastern Mediterranean and Southeast Asia 1. In most endemic areas in Southeast Asia, P. knowlesi has been reported to cause a majority of malaria cases 3. According to the WHO Meeting report 2017, Malaysia recorded the highest burden of P. knowlesi (69% of total reported cases, mostly mono-infection) in 2016, which mostly affected men than women (about 80%) with more cases occurred among adults aged over 55 years old 2. P. knowlesi cases were mostly reported in Sabah and Sarawak of Malaysian Borneo and other states of Peninsular Malaysia including Kelantan, Pahang, Johor, Terengganu, Selangor, Kedah, Penang, Perak and Melaka 1, 4, 5, 6, 7, 8. The natural hosts of P. knowlesi are long-tailed (Macaca fascicularis) and pig-tailed (Macaca nemestrina) macaques 9, 10, 11, 12. Warren et al., (1970) stated that knowlesi malaria was a rare zoonosis of humans after the first description of P. knowlesi human infection was revealed in 1965 by Chin et al., (1965) 13, 14.
However, more human cases of this simian parasite have been identified after a large focus of apparent P. malariae cases in Kapit, Sarawak was investigated by Singh et al., (2004) using a molecular technique 15. By microscopic examination, a band form appearance of late trophozoites of P. knowlesi has been frequently misdiagnosed as P. malariae, and its early trophozoites have frequently been misidentified as P. falciparum due to similar characteristics such as the presence of double chromatin dots, multiple - infected erythrocytes and appliqué forms 16, 17, 18, 19. Since P. knowlesi is now the dominant malaria parasite infecting humans in Southeast Asia and two times more prevalent than P. falciparum or P. vivax 7, if left untreated, it can result in a severe or fatal disease characterized by acute renal failure, acute respiratory distress syndrome and shock 20, 21. Therefore, knowlesi malaria has become one of the healthcare emergencies in most Southeast Asian countries including Malaysia 22.
Studies of many aspects of P. knowlesi biology have posed an increasingly important challenge. This is partly due to the need to grow the parasite in its macaque host or in-vitro using macaque blood 17, 23, 24. These requirements have restricted studies to laboratories with access to macaques or macaque blood. The recent attempt to grow and proliferate P. knowlesi in-vitro in human red blood cells (RBCs) is, therefore, a substantial step towards expanding research on P. knowlesi 17, 25, 26. In this review, we discuss technical developments of the P. knowlesi in-vitro culture system and how this system can be developed based on a few current approaches that have been used thus far. We also highlight future potentials of the available human-adapted P. knowlesi parasite lines.
Establishment of the Continuous in-vitro Culture of P. knowlesi: Since the maintenance of P. knowlesi in-vitro in rhesus RBCs for several intraerythrocytic cycles was achieved in 1945, 27 attempts to develop a continuous in-vitro culture for this malaria parasite have never ended 28. The long-term in-vitro culture system would allow full analysis of parasite-host cell interactions 29, improve understanding of the biology of P. knowlesi such as the mechanism of invasion 30, 31 and resistance markers 32, and contribute to the development of new anti-malarial drugs and vaccines 31, 33, 34, 35. The study by Ball et al., (1945) indicated that target cells of P. knowlesi are not restricted to a certain age in macaques, however, in humans, it was found that P. knowlesi mainly invades reticulocytes 17, 27. Previous attempts showed that P. knowlesi failed to be maintained exclusively in human blood 25, 29.
The direct culture in 100% human RBCs resulted in very low growth rates and a complete loss of parasites within a week 25. Similarly, Lim et al., (2013) showed that P. knowlesi was poorly proliferated in pooled human blood and had a decreased invasion efficiency into older RBCs 36. Thus, the predilection for reticulocytes has been a major obstacle to establish a continuous in-vitro culture for P. knowlesi as these young RBCs circulate in peripheral blood at a very low concentration (0.5-1% of total RBCs) and for a very short time (24 h) 26. Besides, a large quantity of reticulocytes is required to maintain a continuous culture and obtain an efficient parasite invasion. It was evidenced when P. knowlesi was cultured in blood enriched with more than 8% reticulocytes, increasing parasitemia and propagation 36. The continuous culture was also successfully established and maintained for up to six months.
Potential Use of CD34+ Hematopoietic Stem Cell (HSC)-Derived Reticulocytes for Continuous in-vitro Culture of P. knowlesi: As reticulocytes represent only 0.5-1% of total RBCs in the bloodstream and have a short lifespan prior to maturation 26, collecting sufficient reticulocytes from peripheral blood (PB) to maintain a P. knowlesi or P. vivax culture in-vitro is nearly impossible 28. P. vivax has been shown to have a close phylogenetic relationship to P. knowlesi 37. Furthermore, techniques to concentrate reticulocytes collected from PB using percoll centrifugation, several washing and concentration steps could damage the cells, thus affect invasion efficiency 34, 38.
In an attempt to overcome this hurdle, several approaches have used hematopoietic stem cells (HSCs) isolated from either umbilical cord blood (UCB), bone marrow (BM) or PB as potential resources to generate higher production of reticulocytes in-vitro for parasite invasion 26, 34, 39, 40. The culture systems include the application of specific cytokines and either co-culture the HSCs with feeder cells (i.e., human mesenchymal stem cells) 41, 42, 43, 44 to mimic the medullar micro-environment or without feeder cells 43, 45. With sequential addition of specific growth factors (GFs) such as stem cell factors (SCF), interleukin-3 (IL-3), hydrocortisone and erythropoietin (EPO) in CD34+ HSC differentiation medium, the parasite culture could be maintained for a longer period in the presence of reticulocytes derived from CD34+ HSCs 34, 39.
Although HSC - derived reticulocytes need approximately two weeks to mature rather than the use of immediately available reticulocytes, the former resource assures a more homogeneous and standardized cell population 34, 46, 47. Furuya and his colleagues have improved the method of HSC culture to produce a higher percentage of reticule-cytes by using cryopreserved erythroblasts frozen after 8-day cultivation of UCB-isolated HSCs. The method allows the recovery of reticulocytes in a shorter time than with continuous stem cell culture. Moreover, a substantial number of reticulocytes (up to 0.8% of the total cells) are successfully invaded by P. vivax following 24 h post-cultivation 48. Due to the similarities between P. knowlesi and P. vivax regarding their invasion pathways 33, genetics 49, 50, hosts and target cells 51, 52, these approaches would provide insights into the development of long-term in-vitro culture system for P. knowlesi.
Cryopreservation of Reticulocytes and Malaria Parasite Isolates: Cryopreservation is a process of preserving the biological function of intact living cells or tissues by freezing and storing the material below -80 °C typically at or near the temperature of liquid nitrogen (-196 °C) 53. This technique has been used in Plasmodium studies to allow research to be carried out in laboratories with limited access to fresh parasite isolates 54. This technique facilitates more research groups working on this field and increases chances for major discoveries 55. Among the cryopreservation solutions that have been used in previous studies are glycerolyte solution, medium containing glycerol and sorbitol, and IMDM/10% DMSO/40% FCS solution 48, 56.
Noulin et al., (2012) reported a reliable cryo-preservation protocol for HSC-derived reticulocytes that could be invaded by cryopreserved P. vivax or P. falciparum isolates. More than 70% of cryopreserved cells were remained viable and stable compared to the control cells measured before cryopreservation 34. Another study by Borlon et al., (2012) showed that the invasion efficiency of both cryopreserved parasite isolates and reticulocytes was similar to those obtained with fresh samples. They were also able to maintain the culture for up to 10 days 54. These findings show that cryopreservation of reticulocytes did not affect cell stability as they matured normally and were still viable and able to support parasite growth and invasion 34, 54. The cryopreservation method could be easily replicated in laboratories outside endemic areas and substantially contribute to the development of a continuous in-vitro culture of P. knowlesi in the future.
Invasion Mechanism of P. knowlesi: The invasion mechanism of P. knowlesi involves the interaction of a specific ligand presented on the merozoite surface known as Duffy binding proteins (DBPs) 57 and a receptor available on human RBCs namely Duffy antigen receptor for chemokines (DARC) 58. The invasion depends largely on the availability of DARC because no invasion was observed in Duffy-negative RBCs 25. The level of DARC on mature RBCs is reduced compared to that on reticulocytes 25, which possibly explains the predilection of P. knowlesi for reticulocytes. Besides Duffy binding protein, the reticulocyte binding-like proteins (RBLs), another important ligand family, also contribute to the successful invasion of human RBCs 49, 59.
The RBL proteins expressed by P. knowlesi merozoites have been identified as normocyte binding proteins, PkNBPXa and PkNBPXb 57, 60, 61. Unlike PkNBPXb, PkNBPXa binds to not only macaque cells but also human RBCs 60. Therefore, the availability of human-adapted P. knowlesi line would provide a platform to elucidate the invasion mechanism and hence, facilitates in the improvement of strategies to control knowlesi malaria.
The Similarities of P. knowlesi and P. vivax: P. knowlesi is an ideal model for better understanding the various biological aspects of P. vivax (e.g., genetics, invasion and relapse mechanism, drug resistance) 17, 62. Historically, P. knowlesi shares a few common biological aspects with P. vivax; both parasites were found to invade mainly human reticulocytes 63 and use DARC to invade the reticulocytes 62. The gene sequence of P. knowlesi and P. vivax showed a near perfect synteny scattered with expansions of species-specific genes 37, 64. Thus, in-depth study of P. knowlesi could provide an insight into P. vivax biology and the subsequent discovery of diagnostic tools, drugs and vaccines 17, 62.
Adaptation of P. knowlesi to Continuous in-vitro Culture in Human Erythrocytes: Many attempts have been made to adapt P. knowlesi to stably proliferate in human RBCs in-vitro. However, due to its low replication rates, P. knowlesi has failed to stably grow in human RBCs alone 65. This obstacle has been overcome by slowly growing P. knowlesi in a mixture of macaque and human RBCs 25, 36. Following an initial adaptation in human RBCs, the parasites proliferation rates increased further from 2 fold to 5 fold per day 25. In their report, Moon and his colleagues managed to produce one human-adapted P. knowlesi line known as P. knowlesi A1.H1 (PkA1-H.1) line that has been successfully adapted to continuous culture in-vitro, providing an in-vitro model suitable for further study on P. knowlesi. A major step towards adaptation involves a change in host cell preference for invasion 25.
While not restricted to cells of a certain age in macaques, P. knowlesi was found to invade mainly young RBCs in humans. In contrast, the human-adapted line had increased invasion efficiency into older RBCs, providing access to a wider range of suitable host cells 17, 25. The invasion of adapted P. knowlesi lines were still DARC dependent 25. However, further investigation is necessary on the exact receptors involved in the later stage of invasion as the DARC level on blood cells diminishes as they mature 17. Therefore, the availability of human RBC-adapted P. knowlesi lines and the analyses of adaptation mechanism would enable the understanding of the parasite biology and the pathophysiology of knowlesi malaria in humans.
The Implications of Adaptation Success to Malaria Study: A successful establishment of continuous P. knowlesi in-vitro culture and adaptation in human RBCs would offer an ideal system for various implications to malaria research. The development of several advanced tools and technologies for use in other Plasmodium studies such as P. falciparum could be readily adapted for use in P. knowlesi 17. The application of advanced microscopy technologies such as real-time imaging of invasion 66, super-resolution microscopy 67 and long-term live microscopy 17 to the P. knowlesi system will be particularly fruitful. The combination of high transfection efficiency and the ability to culture P. knowlesi in human RBCs will be ideal for the establishment of high-throughput analysis of gene functions 29 and novel reverse genetics, which can be used to investigate the role of RBC receptors in P. knowlesi invasion 68.
The application of several knockout/knockdown systems such as ligand-regulatable FKBP protein destabilization domains (ddFKBP) 69, 70 and the DiCre conditional recombinase system 71 in P. knowlesi will be beneficial in determining the functions of essential blood stage proteins. Likewise, high-efficiency genome editing tools such as TALEN (transcription activator-like effector nucleases) 72, CRISPR (clustered regularly interspaced short palindromic repeat)-Cas system 73 and zinc-finger nucleases 74 could be used to facilitate genomic integration of DNA constructs in P. knowlesi 17.
Also, human RBC-adapted P. knowlesi would allow a comprehensive study of invasion mechanism hence would prevent infection and suppress re-emergent blood stage parasite via the development of new anti-malarial drugs and vaccines 36, 75, 76. Taken together, malaria research could be expanded further following successful adaptation and development of a long-term P. knowlesi in-vitro culture.
ACKNOWLEDGEMENT: We would like to thank Universiti Sains Malaysia (USM) for the Research University Grant given (USM RUI Grant No. 1001/PPSK/812201).
CONFLICT OF INTEREST: The authors declare no conflict of interest.
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How to cite this article:
Mohamad FS and Abu-Bakar N: Towards successful adaptation of Plasmodium knowlesi to long-term in-vitro culture in human erythrocytes. Int J Pharm Sci & Res 2019; 10(6): 2663-69. doi: 10.13040/IJPSR.0975-8232.10(6).2663-69.
All © 2013 are reserved by International Journal of Pharmaceutical Sciences and Research. This Journal licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.
F. S. Mohamad and N. Abu-Bakar *
School of Health Sciences, Health Campus, Universiti Sains Malaysia, Kubang Kerian, Kelantan, Malaysia.
04 September 2018
18 December 2018
04 April 2019
01 June 2019