Environmental Constraints Guide Migration of Malaria Parasites During Transmission

Overview

Journal PLoS Pathog

Specialty Microbiology

Date 2011 Jun 24

PMID 21698220

Citations 34

Authors

Janina Kristin Hellmann

Sylvia Munter

Mikhail Kudryashev

Simon Schulz

Kirsten Heiss

Ann-Kristin Muller

Kai Matuschewski

Joachim P Spatz

Ulrich S Schwarz

Friedrich Frischknecht

Affiliations

Soon will be listed here.

Abstract

Migrating cells are guided in complex environments mainly by chemotaxis or structural cues presented by the surrounding tissue. During transmission of malaria, parasite motility in the skin is important for Plasmodium sporozoites to reach the blood circulation. Here we show that sporozoite migration varies in different skin environments the parasite encounters at the arbitrary sites of the mosquito bite. In order to systematically examine how sporozoite migration depends on the structure of the environment, we studied it in micro-fabricated obstacle arrays. The trajectories observed in vivo and in vitro closely resemble each other suggesting that structural constraints can be sufficient to guide Plasmodium sporozoites in complex environments. Sporozoite speed in different environments is optimized for migration and correlates with persistence length and dispersal. However, this correlation breaks down in mutant sporozoites that show adhesion impairment due to the lack of TRAP-like protein (TLP) on their surfaces. This may explain their delay in infecting the host. The flexibility of sporozoite adaption to different environments and a favorable speed for optimal dispersal ensures efficient host switching during malaria transmission.

Citing Articles

Submicrometre spatiotemporal characterization of the Toxoplasma adhesion strategy for gliding motility.

Vigetti L, Touquet B, Debarre D, Rose T, Bureau L, Abdallah D Nat Microbiol. 2024; 9(12):3148-3164.

PMID: 39496912 DOI: 10.1038/s41564-024-01818-3.

sporozoite shows distinct motility patterns in responses to three-dimensional environments.

Liu Z, Li S, Anantha P, Thanakornsombut T, Wu L, Chen J iScience. 2024; 27(8):110463.

PMID: 39129829 PMC: 11315120. DOI: 10.1016/j.isci.2024.110463.

A geometrical theory of gliding motility based on cell shape and surface flow.

Lettermann L, Ziebert F, Schwarz U Proc Natl Acad Sci U S A. 2024; 121(30):e2410708121.

PMID: 39028692 PMC: 11287263. DOI: 10.1073/pnas.2410708121.

Deformability and collision-induced reorientation enhance cell topotaxis in dense microenvironments.

van Steijn L, Wondergem J, Schakenraad K, Heinrich D, Merks R Biophys J. 2023; 122(13):2791-2807.

PMID: 37291829 PMC: 10397819. DOI: 10.1016/j.bpj.2023.06.001.

Screening the Pathogen Box for Inhibition of Plasmodium falciparum Sporozoite Motility Reveals a Critical Role for Kinases in Transmission Stages.

Kanatani S, Elahi R, Kanchanabhogin S, Vartak N, Tripathi A, Prigge S Antimicrob Agents Chemother. 2022; 66(9):e0041822.

PMID: 35943271 PMC: 9487509. DOI: 10.1128/aac.00418-22.

References

Combe A, Moreira C, Ackerman S, Thiberge S, Templeton T, Menard R . TREP, a novel protein necessary for gliding motility of the malaria sporozoite. Int J Parasitol. 2008; 39(4):489-96. DOI: 10.1016/j.ijpara.2008.10.004. View

Saxton M . Single-particle tracking: the distribution of diffusion coefficients. Biophys J. 1997; 72(4):1744-53. PMC: 1184368. DOI: 10.1016/S0006-3495(97)78820-9. View

Borgne M, Ladi E, Dzhagalov I, Herzmark P, Liao Y, Chakraborty A . The impact of negative selection on thymocyte migration in the medulla. Nat Immunol. 2009; 10(8):823-30. PMC: 2793676. DOI: 10.1038/ni.1761. View

Amino R, Giovannini D, Thiberge S, Gueirard P, Boisson B, Dubremetz J . Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe. 2008; 3(2):88-96. DOI: 10.1016/j.chom.2007.12.007. View

Eisenbach M . A hitchhiker's guide through advances and conceptual changes in chemotaxis. J Cell Physiol. 2007; 213(3):574-80. DOI: 10.1002/jcp.21238. View

Steinbuechel M, Matuschewski K . Role for the Plasmodium sporozoite-specific transmembrane protein S6 in parasite motility and efficient malaria transmission. Cell Microbiol. 2008; 11(2):279-88. PMC: 2688672. DOI: 10.1111/j.1462-5822.2008.01252.x. View

Munter S, Sabass B, Selhuber-Unkel C, Kudryashev M, Hegge S, Engel U . Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites. Cell Host Microbe. 2009; 6(6):551-62. DOI: 10.1016/j.chom.2009.11.007. View

Frischknecht F . The skin as interface in the transmission of arthropod-borne pathogens. Cell Microbiol. 2007; 9(7):1630-40. DOI: 10.1111/j.1462-5822.2007.00955.x. View

Matuschewski K, Nunes A, Nussenzweig V, Menard R . Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 2002; 21(7):1597-606. PMC: 125935. DOI: 10.1093/emboj/21.7.1597. View

10.

Ejigiri I, Sinnis P . Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Curr Opin Microbiol. 2009; 12(4):401-7. PMC: 2725221. DOI: 10.1016/j.mib.2009.06.006. View

11.

Guiguemde W, Shelat A, Bouck D, Duffy S, Crowther G, Davis P . Chemical genetics of Plasmodium falciparum. Nature. 2010; 465(7296):311-5. PMC: 2874979. DOI: 10.1038/nature09099. View

12.

Vanderberg J . Studies on the motility of Plasmodium sporozoites. J Protozool. 1974; 21(4):527-37. DOI: 10.1111/j.1550-7408.1974.tb03693.x. View

13.

Hellmann J, Munter S, Wink M, Frischknecht F . Synergistic and additive effects of epigallocatechin gallate and digitonin on Plasmodium sporozoite survival and motility. PLoS One. 2010; 5(1):e8682. PMC: 2800191. DOI: 10.1371/journal.pone.0008682. View

14.

Mikolajczak S, Silva-Rivera H, Peng X, Tarun A, Camargo N, Jacobs-Lorena V . Distinct malaria parasite sporozoites reveal transcriptional changes that cause differential tissue infection competence in the mosquito vector and mammalian host. Mol Cell Biol. 2008; 28(20):6196-207. PMC: 2577418. DOI: 10.1128/MCB.00553-08. View

15.

Miller M, Wei S, Cahalan M, Parker I . Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc Natl Acad Sci U S A. 2003; 100(5):2604-9. PMC: 151387. DOI: 10.1073/pnas.2628040100. View

16.

Beier J . Malaria parasite development in mosquitoes. Annu Rev Entomol. 1998; 43:519-43. DOI: 10.1146/annurev.ento.43.1.519. View

17.

Ishino T, Yano K, Chinzei Y, Yuda M . Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol. 2004; 2(1):E4. PMC: 314464. DOI: 10.1371/journal.pbio.0020004. View

18.

Amino R, Thiberge S, Martin B, Celli S, Shorte S, Frischknecht F . Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med. 2006; 12(2):220-4. DOI: 10.1038/nm1350. View

19.

Moreira C, Templeton T, Lavazec C, Hayward R, Hobbs C, Kroeze H . The Plasmodium TRAP/MIC2 family member, TRAP-Like Protein (TLP), is involved in tissue traversal by sporozoites. Cell Microbiol. 2008; 10(7):1505-16. PMC: 3937816. DOI: 10.1111/j.1462-5822.2008.01143.x. View

20.

Hegge S, Munter S, Steinbuchel M, Heiss K, Engel U, Matuschewski K . Multistep adhesion of Plasmodium sporozoites. FASEB J. 2010; 24(7):2222-34. DOI: 10.1096/fj.09-148700. View