Longitudinal analysis of plasmodium sporozoite motility in the dermis reveals component of blood vessel recognition

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages

  Hopp, Christine S ^a   Chiou, Kevin ^b   Ragheb, Daniel R T ^a   Salman, Ahmed M ^c   Khan, Shahid M ^c   Liu, Andrea J ^b   Sinnis, Photini ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN;

ANOPHELES STEPHENSI; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; DATA ANALYSIS; DERMIS; GENE MUTATION; GENETIC TRANSFECTION; HOST PARASITE INTERACTION; IMMUNOFLUORESCENCE; MICROSCOPY; MOSQUITO BITE; MOUSE; NEEDLE; NONHUMAN; PARASITE LOAD; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SPOROZOITE; VASCULAR ENDOTHELIUM; VASCULARIZATION; WESTERN BLOTTING; ANIMAL; ANOPHELES; DISEASE MODEL; LOCOMOTION; MALARIA; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM;

ANIMALS; ANOPHELES; BLOOD VESSELS; DERMIS; DISEASE MODELS, ANIMAL; LOCOMOTION; MALARIA; MICE; MICROSCOPY; PLASMODIUM; SPOROZOITES;

EID: 84943770534     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07789     Document Type: Article

References (28)

1. Amino R, Giovannini D, Thiberge S, Gueirard P, Boisson B, Dubremetz JF, Prevost MC, Ishino T, Yuda M, Menard R. 2008. Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host & Microbe 3:88–96. doi: 10.1016/j.chom.2007.12.007.
2. Amino R, Thiberge S, Blazquez S, Baldacci P, Renaud O, Shorte S, Me´ nard R. 2007. Imaging malaria sporozoites in the dermis of the mammalian host. Nature Protocols 2:1705–1712. doi: 10.1038/nprot.2007.120.
3. Amino R, Thiberge S, Martin B, Celli S, Shorte S, Frischknecht F, Menard R. 2006. Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nature Medicine 12:220–224. doi: 10.1038/nm1350.
4. Battista A, Frischknecht F, Schwarz US. 2014. A geometrical model for malaria parasite migration in structured environments. Physical Review. E, Statistical, Nonlinear, and Soft Matter Physics 90:042720. doi: 10.1103/PhysRevE.90.042720.
5. Beltman JB, Maree AF, de Boer RJ. 2009. Analysing immune cell migration. Nature Reviews. Immunology 9:789–798. doi: 10.1038/nri2638.
6. Braverman IM. 1997. The cutaneous microcirculation: ultrastructure and microanatomical organization. Microcirculation 4:329–340. doi: 10.3109/10739689709146797.
7. Bruna-Romero O, Hafalla JC, Gonzalez-Aseguinolaza G, Sano G, Tsuji M, Zavala F. 2001. Detection of malaria liverstages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. International Journal for Parasitology 31:1499–1502. doi: 10.1016/S0020-7519(01)00265-X.
8. Coppi A, Natarajan R, Pradel G, Bennett BL, James ER, Roggero MA, Corradin G, Persson C, Tewari R, Sinnis P. 2011. The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito tomammalian host. The Journal of Experimental Medicine 208:341–356. doi: 10.1084/jem.20101488.
9. Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P. 2005. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. The Journal of Experimental Medicine 201:27–33. doi: 10.1084/jem.20040989.
10. Ejigiri I, Ragheb DR, Pino P, Coppi A, Bennett BL, Soldati-Favre D, Sinnis P. 2012. Shedding of TRAP by a rhomboid protease from the malaria sporozoite surface is essential for gliding motility and sporozoite infectivity. PLOS Pathogens 8:e1002725. doi: 10.1371/journal.ppat.1002725.
11. Foquet L, Hermsen CC, van Gemert GJ, Van Braeckel E, Weening KE, Sauerwein R, Meuleman P, Leroux-Roels G. 2014. Vaccine-induced monoclonal antibodies targeting circumsporozoite protein prevent Plasmodium falciparum infection. The Journal of Clinical Investigation 124:140–144. doi: 10.1172/JCI70349.
12. Formaglio P, Tavares J, Menard R, Amino R. 2014. Loss of host cell plasma membrane integrity following cell traversal by Plasmodium sporozoites in the skin. Parasitology International 63:237–244. doi: 10.1016/j.parint.2013.07.009.
13. Harris TH, Banigan EJ, Christian DA, Konradt C, Tait Wojno ED, Norose K, Wilson EH, John B, Weninger W, Luster AD, Liu AJ, Hunter CA. 2012. Generalized Le´ vy walks and the role of chemokines in migration of effector CD8+T cells. Nature 486:545–548. doi: 10.1038/nature11098.
14. Hellmann JK, Munter S, Kudryashev M, Schulz S, Heiss K, Muller AK, Matuschewski K, Spatz JP, Schwarz US, Frischknecht F. 2011. Environmental constraints guide migration of malaria parasites during transmission. PLOS Pathogens 7:e1002080. doi: 10.1371/journal.ppat.1002080.
15. Janse CJ, Ramesar J, Waters AP. 2006. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nature Protocols 1:346–356. doi: 10.1038/nprot.2006.53.
16. Kan A, Tan YH, Angrisano F, Hanssen E, Rogers KL, Whitehead L, Mollard VP, Cozijnsen A, Delves MJ, Crawford S, Sinden RE, McFadden GI, Leckie C, Bailey J, Baum J. 2014. Quantitative analysis of Plasmodium ookinete motion in three-dimensions suggests a critical role for cell shape in the biomechanics of malaria parasite gliding motility. Cellular Microbiology 16:734–750. doi: 10.1111/cmi.12283.
17. Kilarski WW, Guc E, Teo JC, Oliver SR, Lund AW, Swartz MA. 2013. Intravital immunofluorescence for visualizing the microcirculatory and immune microenvironments in the mouse ear dermis. PLOS ONE 8:e57135. doi: 10.1371/journal.pone.0057135.
18. Lin JW, Annoura T, Sajid M, Chevalley-Maurel S, Ramesar J, Klop O, Franke-Fayard BM, Janse CJ, Khan SM. 2011. A novel ‘gene insertion/marker out’ (GIMO) method for transgene expression and gene complementation in rodent malaria parasites. PLOS ONE 6:e29289. doi: 10.1371/journal.pone.0029289.
19. Mueller AK, Camargo N, Kaiser K, Andorfer C, Frevert U, Matuschewski K, Kappe SH. 2005. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proceedings of the National Academy of Sciences of USA 102:3022–3027. doi: 10.1073/pnas.0408442102.
20. Munter S, Sabass B, Selhuber-Unkel C, Kudryashev M, Hegge S, Engel U, Spatz JP, Matuschewski K, Schwarz US, Frischknecht F. 2009. Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites. Cell Host & Microbe 6:551–562. doi: 10.1016/j.chom.2009.11.007.
21. Orr RY, Philip N, Waters AP. 2012. Improved negative selection protocol for Plasmodium berghei in the rodent malarial model. Malaria Journal 11:103. doi: 10.1186/1475-2875-11-103.
22. Radtke AJ, Kastenmu ller W, Espinosa DA, Gerner MY, Tse SW, Sinnis P, Germain RN, Zavala FP, Cockburn IA. 2015. Lymph-node resident CD8α+ dendritic cells capture antigens from migratory malaria sporozoites and induce CD8+ T cell responses. PLOS Pathogens 11:e1004637. doi: 10.1371/journal.ppat.1004637.
23. Sarkisyan G, Cahalan SM, Gonzalez-Cabrera PJ, Leaf NB, Rosen H. 2012. Real-time differential labeling of blood, interstitium, and lymphatic and single-field analysis of vasculature dynamics in vivo. American Journal of Physiology. Cell Physiology 302:C1460–C1468. doi: 10.1152/ajpcell.00382.2011.
24. Sinnis P, Zavala F. 2012. The skin: where malaria infection and the host immune response begin. Seminars in Immunopathology 34:787–792. doi: 10.1007/s00281-012-0345-5.
25. Vanderberg JP. 1974. Studies on the motility of Plasmodium sporozoites. The Journal of Protozoology 21:527–537. doi: 10.1111/j.1550-7408.1974.tb03693.x.
26. Vanderberg JP, Frevert U. 2004. Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. International Journal for Parasitology 34:991–996. doi: 10.1016/j.ijpara.2004.05.005.
27. Yen A, Braverman IM. 1976. Ultrastructure of the human dermal microcirculation: the horizontal plexus of the papillary dermis. The Journal of Investigative Dermatology 66:131–142. doi: 10.1111/1523-1747.ep12481678.
28. Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M. 1980. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207:71–73. doi: 10.1126/science.6985745.