SSP3 is a novel Plasmodium yoelii sporozoite surface protein with a role in gliding motility

Anke Harupa, Brandon Wilder, Viswanathan Lakshmanan, Nadia Arang, Alyse N. Douglass, Brian G. Oliver, Andrew B. Stuart, D. Noah Sather, Scott E. Lindner, Kevin Hybiske, Motomi Torii, Stefan H.I. Kappe

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Plasmodium sporozoites develop within oocysts in the mosquito midgut wall and then migrate to the salivary glands. After transmission, they embark on a complex journey to the mammalian liver, where they infect hepatocytes. Proteins on the sporozoite surface likely mediate multiple steps of this journey, yet only a few sporozoite surface proteins have been described. Here, we characterize a novel, conserved sporozoite surface protein (SSP3) in the rodent malaria parasite Plasmodium yoelii. SSP3 is a putative type I transmembrane protein unique to Plasmodium. By using epitope tagging and SSP3-specific antibodies in conjunction with immunofluorescence microscopy, we showed that SSP3 is expressed in mosquito midgut oocyst sporozoites, exhibiting an intracellular localization. In sporozoites derived from the mosquito salivary glands, however, SSP3 localized predominantly to the sporozoite surface as determined by immunoelectron microscopy. However, the ectodomain of SSP3 appeared to be inaccessible to antibodies in nonpermeabilized salivary gland sporozoites. Antibody-induced shedding of the major surface protein circumsporozoite protein (CSP) exposed the SSP3 ectodomain to antibodies in some sporozoites. Targeted deletion of SSP3 adversely affected in vitro sporozoite gliding motility, which, surprisingly, impacted neither their cell traversal capacity, host cell invasion in vitro, nor infectivity in vivo. Together, these data reveal a previously unappreciated complexity of the Plasmodium sporozoite surface proteome and the roles of surface proteins in distinct biological activities of sporozoites.

Original languageEnglish (US)
Pages (from-to)4643-4653
Number of pages11
JournalInfection and Immunity
Volume82
Issue number11
DOIs
StatePublished - Jan 1 2014
Externally publishedYes

Fingerprint

Plasmodium yoelii
Sporozoites
Membrane Proteins
Plasmodium
Salivary Glands
Culicidae
Oocysts
Antibodies
Proteins
Immunoelectron Microscopy
Proteome
Fluorescence Microscopy
Malaria

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

Harupa, A., Wilder, B., Lakshmanan, V., Arang, N., Douglass, A. N., Oliver, B. G., ... Kappe, S. H. I. (2014). SSP3 is a novel Plasmodium yoelii sporozoite surface protein with a role in gliding motility. Infection and Immunity, 82(11), 4643-4653. https://doi.org/10.1128/IAI.01800-14

SSP3 is a novel Plasmodium yoelii sporozoite surface protein with a role in gliding motility. / Harupa, Anke; Wilder, Brandon; Lakshmanan, Viswanathan; Arang, Nadia; Douglass, Alyse N.; Oliver, Brian G.; Stuart, Andrew B.; Noah Sather, D.; Lindner, Scott E.; Hybiske, Kevin; Torii, Motomi; Kappe, Stefan H.I.

In: Infection and Immunity, Vol. 82, No. 11, 01.01.2014, p. 4643-4653.

Research output: Contribution to journalArticle

Harupa, A, Wilder, B, Lakshmanan, V, Arang, N, Douglass, AN, Oliver, BG, Stuart, AB, Noah Sather, D, Lindner, SE, Hybiske, K, Torii, M & Kappe, SHI 2014, 'SSP3 is a novel Plasmodium yoelii sporozoite surface protein with a role in gliding motility', Infection and Immunity, vol. 82, no. 11, pp. 4643-4653. https://doi.org/10.1128/IAI.01800-14
Harupa, Anke ; Wilder, Brandon ; Lakshmanan, Viswanathan ; Arang, Nadia ; Douglass, Alyse N. ; Oliver, Brian G. ; Stuart, Andrew B. ; Noah Sather, D. ; Lindner, Scott E. ; Hybiske, Kevin ; Torii, Motomi ; Kappe, Stefan H.I. / SSP3 is a novel Plasmodium yoelii sporozoite surface protein with a role in gliding motility. In: Infection and Immunity. 2014 ; Vol. 82, No. 11. pp. 4643-4653.
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AU - Stuart, Andrew B.

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