Asparagine Repeats in Plasmodium falciparum Proteins: Good for Nothing?

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Muralidharan, Vasant ^a   Goldberg, Daniel E ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; HEAT SHOCK PROTEIN 110; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; GENOME; HUMAN; NONHUMAN; PLASMODIUM FALCIPARUM; PREVALENCE; PROTEIN FUNCTION; GENETICS; TRINUCLEOTIDE REPEAT;

ASPARAGINE; GENOME, PROTOZOAN; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; TRINUCLEOTIDE REPEATS;

EID: 84883370468     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003488     Document Type: Article

References (27)

1. Cibulskis RE, Aregawi M, Williams R, Otten M, Dye C, (2011) Worldwide incidence of malaria in 2009: estimates, time trends, and a critique of methods. PLoS Med 8: e1001142 doi:10.1371/journal.pmed.1001142.
2. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
3. Aravind L, Iyer LM, Wellems TE, Miller LH, (2003) Plasmodium biology: genomic gleanings. Cell 115: 771-785.
4. Kemp DJ, Coppel RL, Anders RF, (1987) Repetitive proteins and genes of malaria. Annu Rev Microbiol 41: 181-208.
5. Wootton JC, (1994) Non-globular domains in protein sequences: automated segmentation using complexity measures. Comput Chem 18: 269-285.
6. Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R, et al. (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435: 43-57.
7. Singh GP, Chandra BR, Bhattacharya A, Akhouri RR, Singh SK, et al. (2004) Hyper-expansion of asparagines correlates with an abundance of proteins with prion-like domains in Plasmodium falciparum. Mol Biochem Parasitol 137: 307-319.
8. Zilversmit MM, Volkman SK, DePristo MA, Wirth DF, Awadalla P, et al. (2010) Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Mol Biol Evol 27: 2198-2209.
9. Halfmann R, Alberti S, Krishnan R, Lyle N, O'Donnell CW, et al. (2011) Opposing effects of glutamine and asparagine govern prion formation by intrinsically disordered proteins. Mol Cell 43: 72-84.
10. Alberti S, Halfmann R, King O, Kapila A, Lindquist S, (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137: 146-158.
11. Fowler DM, Koulov AV, Balch WE, Kelly JW, (2007) Functional amyloid - from bacteria to humans. Trends Biochem Sci 32: 217-224.
12. Chiti F, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333-366.
13. Patino MM, Liu JJ, Glover JR, Lindquist S, (1996) Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273: 622-626.
14. Si K, Choi Y-B, White-Grindley E, Majumdar A, Kandel ER, (2010) Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140: 421-435.
15. Hou F, Sun L, Zheng H, Skaug B, Jiang Q-X, et al. (2011) MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146: 448-461.
16. Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, et al. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144: 67-78.
17. Seuring C, Greenwald J, Wasmer C, Wepf R, Saupe SJ, et al. (2012) The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLoS Biol 10: e1001451 doi:10.1371/journal.pbio.1001451.
18. Muralidharan V, Oksman A, Pal P, Lindquist S, Goldberg DE, (2012) Plasmodium falciparum heat shock protein 110 stabilizes the asparagine repeat-rich parasite proteome during malarial fevers. Nat Commun 3: 1310.
19. Frugier M, Bour T, Ayach M, Santos MAS, Rudinger-Thirion J, et al. (2010) Low complexity regions behave as tRNA sponges to help co-translational folding of plasmodial proteins. FEBS Lett 584: 448-454.
20. Verra F, Hughes AL, (1999) Biased amino acid composition in repeat regions of Plasmodium antigens. Mol Biol Evol 16: 627-633.
21. Hughes AL, (2004) The evolution of amino acid repeat arrays in Plasmodium and other organisms. J Mol Evol 59: 528-535.
22. Karlin S, Brocchieri L, Bergman A, Mrazek J, Gentles AJ, (2002) Amino acid runs in eukaryotic proteomes and disease associations. Proc Natl Acad Sci U S A 99: 333-338.
23. Muralidharan V, Oksman A, Iwamoto M, Wandless TJ, Goldberg DE, (2011) Asparagine repeat function in a Plasmodium falciparum protein assessed via a regulatable fluorescent affinity tag. Proc Natl Acad Sci U S A 108: 4411-4416 doi:10.1073/pnas.1018449108.
24. Xue HY, Forsdyke DR, (2003) Low-complexity segments in Plasmodium falciparum proteins are primarily nucleic acid level adaptations. Mol Biochem Parasitol 128: 21-32.
25. Anderson TJC, Patel J, Ferdig MT, (2009) Gene copy number and malaria biology. Trends Parasitol 25: 336-343.
26. Dalby AR, (2009) A comparative proteomic analysis of the simple amino acid repeat distributions in Plasmodia reveals lineage specific amino acid selection. PLoS ONE 4: e6231 doi:10.1371/journal.pone.0006231.
27. Rutherford SL, Lindquist S, (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.