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Background  Antigenic variation by malaria parasites was first described in  Plasmodium knowlesi , which infects humans and macaque monkeys, and subsequently in  P. falciparum , the most virulent human parasite. The schizont-infected cell agglutination (SICA) variant proteins encoded by the  SICAvar  multigene family in  P. knowlesi , and Erythrocyte Membrane Protein-1 (EMP-1) antigens encoded by the  var  multigene family in  P. falciparum , are expressed at the surface of infected erythrocytes, are associated with virulence, and serve as determinants of naturally acquired immunity. A parental  P. knowlesi  clone, Pk1(A+), and a related progeny clone, Pk1(B+)1+, derived by an  in   vivo  induced variant antigen switch, were defined by the expression of distinct SICA variant protein doublets of 210/190 and 205/200 kDa, respectively. Passage of SICA[+] infected erythrocytes through splenectomized rhesus monkeys results in the SICA[-] phenotype, defined by the lack of surface expression and agglutination with variant specific antisera.    Principal Findings  We have investigated  SICAvar  RNA and protein expression in Pk1(A+), Pk1(B+)1+, and SICA[-] parasites. The Pk1(A+) and Pk1(B+)1+ parasites express different distinct  SICAvar  transcript and protein repertoires. By comparison, SICA[-] parasites are characterized by a vast reduction in  SICAvar  RNA expression, the lack of full-length  SICAvar  transcript signals on northern blots, and correspondingly, the absence of any SICA protein detected by mass spectrometry.    Significance  SICA protein expression may be under transcriptional as well as post-transcriptional control, and we show for the first time that the spleen, an organ central to blood-stage immunity in malaria, exerts an influence on these processes. Furthermore, proteomics has enabled the first in-depth characterization of SICA[+] protein phenotypes and we show that the  in   vivo  switch from Pk1(A+) to Pk1(B+)1+ parasites resulted in a complete change in SICA profiles. These results emphasize the importance of studying antigenic variation in the context of the host environment.

Spleen-Dependent Regulation of Antigenic Variation in Malaria Parasites: Plasmodium knowlesi SICAvar Expression Profiles in Splenic and Asplenic Hosts