Small molecule targeting malaria Merozoite surface protein-1 (MSP-1) prevents host invasion of divergent Plasmodial species

Journal of Infectious Diseases

Volumn 210, Issue 10, 2014, Pages 1616-1626

  Chandramohanadas, Rajesh ^a,b   Russell, Bruce ^c   Liew, Kingsley ^a   Yau, Yin Hoe ^d   Chong, Alvin ^a   Liu, Min ^a   Gunalan, Karthigayan ^d   Raman, Rahul ^e   Renia, Laurent ^f   Nosten, Francois ^g,h   Shochat, Susana Geifman ^d   Dao, Ming ^a,e   Sasisekharan, Ram ^a,e   Suresh, Subra ⁱ   Preiser, Peter ^a,d  

^a SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^b SINGAPORE UNIVERSITY OF TECHNOLOGY AND DESIGN   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e Massachusetts Institute of Technology   (United States)

^f AGENCY FOR SCIENCE   (Singapore)

^g SHOKLO MALARIA RESEARCH UNIT   (Thailand)

^h UNIVERSITY OF OXFORD   (United Kingdom)

ⁱ CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

chemical biology; glycan mimetic small molecules; host invasion; malaria; mass spectrometry; merozoite surface proteins; Plasmodium falciparum; Plasmodium vivax; red blood cell

Indexed keywords

2 BUTYL 5 CHLORO 3 (4 NITRO BENZYL) 3H IMIDAZOLE 4 CARBALDEHYDE; LIGAND; MEROZOITE SURFACE PROTEIN 1; UNCLASSIFIED DRUG; ANTIMALARIAL AGENT;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPUTER MODEL; CONTROLLED STUDY; IN VITRO STUDY; MEROZOITE; MOLECULAR DOCKING; NONHUMAN; PARASITE PHENOMENA AND FUNCTIONS; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SPECIES INVASION; SURFACE PLASMON RESONANCE; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENDOCYTOSIS; HUMAN; ISOLATION AND PURIFICATION;

ANTIMALARIALS; ENDOCYTOSIS; HUMANS; MEROZOITE SURFACE PROTEIN 1; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX;

EID: 84906990531     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu296     Document Type: Article

References (49)

1. Agnandji ST, Lell B, Soulanoudjingar SS, et al. First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. N Engl J Med 2011; 365:1863-75.
2. Murray CJ, Rosenfeld LC, Lim SS, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012; 379:413-31; doi:10.1016/S0140-6736(12)60034-8.
3. Mita T, Tanabe K, Kita K. Spread and evolution of Plasmodium falciparum drug resistance. Parasitol Int 2009; 58:201-9.
4. OBrien C, Henrich PP, Passi N, Fidock DA. Recent clinical and molecular insights into emerging artemisinin resistance in Plasmodium falciparum. Curr Opin Infect Dis 2011; 24:570-7.
5. Breuer WV, Kahane I, Baruch D, Ginsburg H, Cabantchik ZI. Role of internal domains of glycophorin in Plasmodium falciparum invasion of human erythrocytes. Infect Immun 1983; 42:133-40.
6. Mayer DC, Cofie J, Jiang L, et al. Glycophorin B is the erythrocyte receptor of Plasmodium falciparum erythrocyte-binding ligand, EBL-1. Proc Natl Acad Sci U S A 2009; 106:5348-52.
7. Sim BK, Chitnis CE, Wasniowska K, Hadley TJ, Miller LH. Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 1994; 264:1941-4.
8. Duraisingh MT, Maier AG, Triglia T, Cowman AF. Erythrocyte- binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and independent pathways. Proc Natl Acad Sci U S A 2003; 100:4796-801.
9. Spadafora C, Awandare GA, Kopydlowski KM, et al. Complement receptor 1 is a sialic acid-independent erythrocyte receptor of Plasmodium falciparum. PLoS Pathog 2010; 6:e1000968.
10. Langermans JA, Hensmann M, van Gijlswiik M, et al. Preclinical evaluation of a chimeric malaria vaccine candidate in Montanide ISA 720: immunogenicity and safety in rhesus macaques. Hum Vaccin 2006; 2:222-6.
11. Ellis RD, Martin LB, Schaffer D, et al. Phase 1 trial of the Plasmodium falciparum blood stage vaccine MSP1 (42)- C1/Alhydrogel with and without CPG 7909 in malaria nave adults. PLoS One 2010; 5:e8787.
12. Goel VK, Li X, Chen H, Liu SC, Chishti AH, Oh SS. Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes. Proc Natl Acad Sci U S A 2003; 100:5164-9.
13. Child MA, Epp C, Bujard H, Blackman MJ. Regulated maturation of malaria merozoite surface protein-1 is essential for parasite growth. Mol Microbiol 2010; 78:187-202.
14. Holder AA, Blackman MJ, Burghaus PA, et al. A malaria merozoite surface protein (MSP1)-structure, processing and function. Mem Inst Oswaldo Cruz 1992; 87(suppl 3):37-42.
15. Chappel JA, Holder AA. Monoclonal antibodies that inhibit Plasmodium falciparum invasion in vitro recognise the first growth factor-like domain of merozoite surface protein-1. Mol Biochem Parasitol 1993; 60:303-11.
16. Moss DK, Remarque EJ, Faber BW, et al. Plasmodium falciparum 19- kilodalton merozoite surface protein 1 (MSP1)-specific antibodies that interfere with parasite growth in vitro can inhibit MSP1 processing, merozoite invasion, and intracellular parasite development. Infect Immun 2012; 80:1280-7.
17. Dluzewski AR, Ling IT, Hopkins JM, et al. Formation of the food vacuole in Plasmodium falciparum: a potential role for the 19 kDa fragment of merozoite surface protein 1 (MSP1(19)). PLoS One 2008; 3:e3085.
18. Xiao L, Yang C, Patterson PS, Udhayakumar V, Lal AA. Sulfated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes. Infect Immun 1996; 64:1373-8.
19. Kisilevsky R, Crandall I, SzarekWA, et al. Short-chain aliphatic polysulfonates inhibit the entry of Plasmodium into red blood cells. Antimicrob Agents Chemother 2002; 46:2619-26.
20. Adams Y, Freeman C, Schwartz-Albiez R, Ferro V, Parish CR, Andrews KT. Inhibition of Plasmodium falciparum growth in vitro and adhesion to chondroitin-4-sulfate by the heparan sulfate mimetic PI-88 and other sulfated oligosaccharides. Antimicrob Agents Chemother 2006; 50:2850-2.
21. Dalton JP, Hudson D, Adams JH, Miller LH. Blocking of the receptormediated invasion of erythrocytes by Plasmodium knowlesi malaria with sulfated polysaccharides and glycosaminoglycans. Eur J Biochem 1991; 195:789-94.
22. Basseri HR, Doosti S, Akbarzadeh K, Nateghpour M, Whitten MM, Ladoni H. Competency of Anopheles stephensimysorensis strain for Plasmodium vivax and the role of inhibitory carbohydrates to block its sporogenic cycle. Malar J 2008; 7:131.
23. Boyle MJ, Richards JS, Gilson PR, ChaiW, Beeson JG. Interactions with heparin-like molecules during erythrocyte invasion by Plasmodium falciparum merozoites. Blood 2010; 115:4559-68.
24. ODonnell RA, de Koning-Ward TF, Burt RA, et al. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J Exp Med 2001; 193:1403-12.
25. Wu G, Robertson DH, Brooks CL III, Vieth M. Detailed analysis of gridbased molecular docking: a case study of CDOCKER- A CHARMmbased MD docking algorithm. J Comput Chem 2003; 24:1549-62.
26. Venkatachalam CM, Jiang X, Oldfield T, Waldman M. LigandFit: a novel method for the shape-directed rapid docking of ligands to protein active sites. J Mol Graph Model 2003; 21:289-307.
27. Shoichet BK. Virtual screening of chemical libraries. Nature 2004; 432:862-5.
28. Gaonkar SL, Lokanatha Rai KM, Suchetha Shetty N. Microwaveassisted synthesis and evaluation of anti- inflammatory activity of new series of N- substituted 2-butyl-5- chloro- 3 H-imidazole- 4- carbaldehyde derivatives. Med Chem Res 2009; 18:221-30.
29. Morgan WD, Birdsall B, Frenkiel TA, et al. Solution structure of an EGF module pair from the Plasmodium falciparum merozoite surface protein 1. J Mol Biol 1999; 289:113-22.
30. Babon JJ, Morgan WD, Kelly G, Eccleston JF, Feeney J, Holder AA. Structural studies on Plasmodium vivax merozoite surface protein-1. Mol Biochem Parasitol 2007; 153:31-40.
31. Garman SC, Simcoke WN, Stowers AW, Garboczi DN. Structure of the C-terminal domains of merozoite surface protein-1 from Plasmodium knowlesi reveals a novel histidine binding site. J Biol Chem 2003; 278:7264-9.
32. Johnsson B, Lfs S, Lindquist G. Immobilization of proteins to a carboxymethyldextran- modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal Biochem 1991; 198:268-77.
33. Myszka DG. Improving biosensor analysis. J Mol Recognit 1999; 12: 279-84.
34. Wei L, Jiang P, Yau YH, et al. Residual structure in islet amyloid polypeptide mediates its interactions with soluble insulin. Biochemistry 2009; 48:2368-76.
35. Sriprawat K, Kaewpongsri S, Suwanarusk R, et al. Effective and cheap removal of leukocytes and platelets from Plasmodium vivax infected blood. Malar J 2009; 8:115.
36. Russell B, Suwanarusk R, Borlon C, et al. A reliable ex vivo invasion assay of human reticulocytes by Plasmodium vivax. Blood 2011; 118: e74-81.
37. Malleret B, Claser C, Ong AS, et al. A rapid and robust tri-color flow cytometry assay for monitoring malaria parasite development. Sci Rep 2011; 1:118.
38. Ishida K, Wierzba MK, Teruya T, Simizu S, Osada H. Novel heparansulfate mimetic compounds as antitumor agents. Chem Biol 2004; 11:367-77.
39. Basappa , Murugan S, Kavitha CV, et al. A small oxazine compound as an anti-tumor agent: a novel pyranoside mimetic that binds to VEGF, HB- EGF, and TNF-α. Cancer Lett 2010; 297:231-43.
40. Basappa , Sugahara K, Thimmaiah KN, Bid HK, Houghton PJ, Rangappa KS. Anti-tumor activity of a novel HS-mimetic vascular endothelial growth factor binding small molecule. PLoS ONE 2012; 7:e39444. doi:10.1371/journal.pone.0039444.
41. Wilson DW, Crabb BS, Beeson JG. Development of fluorescent Plasmodium falciparum for in vitro growth inhibition assays. Malar J 2010; 9:152.
42. Chandramohanadas R, Davis PH, Beiting DP, et al. Apicomplexan parasites co-opt host calpains to facilitate their escape from infected cells. Science 2009; 324:794-7.
43. Treeck M, Zacherl S, Herrmann S, et al. Functional analysis of the leading malaria vaccine candidate AMA- 1 reveals an essential role for the cytoplasmic domain in the invasion process. PLoS Pathog 2009; 5: e1000322.
44. Boyle MJ,Wilson DW, Richards JS, et al. Isolation of viable Plasmodium falciparum merozoites to define erythrocyte invasion events and advance vaccine and drug development. Proc Natl Acad Sci U S A 2010; 107:14378-83.
45. Han HJ, Park SG, Kim SH, et al. Epidermal growth factor-like motifs 1 and 2 of Plasmodium vivax merozoite surface protein 1 are critical domains in erythrocyte invasion. Biochem Biophys Res Commun 2004; 320:563-70.
46. Iyer J, Grner AC, Rnia L, Snounou G, Preiser PR. Invasion of host cells by malaria parasites: a tale of two protein families. Mol Microbiol 2007; 65:231-49.
47. Greenbaum DC, Baruch A, Grainger M, et al. A role for the protease falcipain 1 in host cell invasion by the human malaria parasite. Science 2002; 298:2002-6.
48. Koussis K, Withers-Martinez C, Yeoh S, et al. A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO J 2009; 28:725-35.
49. Singh S, Alam MM, Pal-Bhowmick I, Brzostowski JA, Chitnis CE. Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog 2010; 6: e1000746.