Plasmodium falciparum liver stage antigen-1 is cross-linked by tissue transglutaminase

Malaria Journal

Volumn 10, Issue , 2011, Pages

  Nicoll, William S ^a   Sacci, John B ^b   Rodolfo, Carlo ^c   Di Giacomo, Giuseppina ^c   Piacentini, Mauro ^c   Holland, Zoe J M ^d   Doerig, Christian ^d   Hollingdale, Michael R ^e   Lanar, David E ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e NMRC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; GLUTAMINE; LIVER ANTIGEN; LIVER STAGE ANTIGEN 1; LYSINE; MONOCLONAL ANTIBODY; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; UNCLASSIFIED DRUG; LIVER STAGE SPECIFIC ANTIGEN, PLASMODIUM; LIVER STAGE-SPECIFIC ANTIGEN, PLASMODIUM; PARASITE ANTIGEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; INVERTED REPEAT; LIVER CELL; MOLECULAR PROBE; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROCESSING; TISSUE SECTION; ANIMAL; FLUORESCENCE MICROSCOPY; HOST PARASITE INTERACTION; LIVER; MALARIA FALCIPARUM; METABOLISM; MOUSE MUTANT; PARASITOLOGY; PATHOGENICITY; PATHOLOGY;

ANIMALS; ANTIGENS, PROTOZOAN; HOST-PARASITE INTERACTIONS; HUMANS; LIVER; MALARIA, FALCIPARUM; MICE; MICE, SCID; MICROSCOPY, FLUORESCENCE; PLASMODIUM FALCIPARUM; TRANSGLUTAMINASES;

EID: 78651552415     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-10-14     Document Type: Article

References (57)

1. A liver-stage-specific antigen of Plasmodium falciparum characterized by gene cloning. C Guerin-Marchand P Druilhe B Galey A Londono J Patarapotikul RL Beaudoin C Dubeaux A Tartar O Mercereau-P (Pubitemid 17125254)
2. T lymphocytes from volunteers immunized with irradiated Plasmodium falciparum sporozoites recognize liver and blood stage malaria antigens. U Krzych JA Lyon T Jareed I Schneider MR Hollingdale DM Gordon WR Ballou, J Immunol 1995 155 4072 4077 7561118
3. Interleukin-10 responses to liver-stage antigen 1 predict human resistance to Plasmodium falciparum. JD Kurtis DE Lanar M Opollo PE Duffy, Infect Immun 1999 67 3424 3429 10377122 (Pubitemid 29291512)
4. Age-dependent enhancement of IFN-gamma responses to Plasmodium falciparum liver stage antigen-1 T cell epitopes. M Bongartz P Rezbach S Borrmann MR Hollingdale PG Kremsner AJ Luty, Parasitol Res 2002 88 1083 1089 10.1007/s00436-002-0703-7 12444460 (Pubitemid 35435572)
5. Plasmodium falciparum liver-stage antigen-1 peptide-specific interferon-gamma responses are not suppressed during uncomplicated malaria in African children. AJ Luty M Bongartz P Rezbach JF Faucher MR Hollingdale PG Kremsner, Eur Cytokine Netw 2001 12 647 653 11781192 (Pubitemid 34062152)
6. HLA-DQB1*0501-restricted Th1 type immune responses to Plasmodium falciparum liver stage antigen 1 protect against malaria anemia and reinfections. J May B Lell AJ Luty CG Meyer PG Kremsner, J Infect Dis 2001 183 168 172 10.1086/317642 11076705 (Pubitemid 32043059)
7. Pre-erythrocytic immunity to Plasmodium falciparum: the case for an LSA-1 vaccine. JD Kurtis MR Hollingdale AJ Luty DE Lanar U Krzych PE Duffy, Trends Parasitol 2001 17 219 223 10.1016/S0169-4758(00)01862-7 11323304 (Pubitemid 32422165)
8. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. AV Hill J Elvin AC Willis M Aidoo CE Allsopp FM Gotch XM Gao M Takiguchi BM Greenwood AR Townsend AJ McMichael H Whittle, Nature 1992 360 434 439 10.1038/360434a0 1280333
9. NYVAC-Pf7: a poxvirus-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. JA Tine DE Lanar DM Smith BT Wellde P Schultheiss LA Ware EB Kauffman RA Wirtz C De Taisne GS Hui SP Chang P Church MR Hollingdale DC Kaslow S Hoffman KP Guito WR Ballou JC Sadoff E Paoletti, Infect Immun 1996 64 3833 3844 8751936 (Pubitemid 26298712)
10. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. CF Ockenhouse PF Sun DE Lanar BT Wellde BT Hall K Kester JA Stoute A Magill U Krzych L Farley RA Wirtz JC Sadoff DC Kaslow S Kumar LW Church JM Crutcher B Wizel S Hoffman A Lalvani AV Hill JA Tine KP Guito C de Taisne R Anders WR Ballou, J Infect Dis 1998 177 1664 1673 10.1086/515331 9607847 (Pubitemid 28243593)
11. Boosting of DNA vaccine-elicited gamma interferon responses in humans by exposure to malaria parasites. R Wang TL Richie MF Baraceros N Rahardjo T Gay JG Banania Y Charoenvit JE Epstein T Luke DA Freilich J Norman SL Hoffman, Infect Immun 2005 73 2863 2872 10.1128/IAI.73.5.2863-2872.2005 15845492 (Pubitemid 40570355)
12. Process development and analysis of liver-stage antigen 1, a preerythrocyte-stage protein-based vaccine for Plasmodium falciparum. CJ Hillier LA Ware A Barbosa E Angov JA Lyon DG Heppner DE Lanar, Infect Immun 2005 73 2109 2115 10.1128/IAI.73.4.2109-2115.2005 15784552 (Pubitemid 40470809)
13. Recombinant Liver Stage Antigen-1 (LSA-1) formulated with AS01 or AS02 is safe, elicits high titer antibody and induces IFN-gamma/IL-2 CD4 + T cells but does not protect against experimental Plasmodium falciparum infection. JF Cummings MD Spring RJ Schwenk CF Ockenhouse KE Kester ME Polhemus DS Walsh IK Yoon C Prosperi LY Juompan DE Lanar U Krzych BT Hall LA Ware VA Stewart J Williams M Dowler RK Nielsen CJ Hillier BK Giersing F Dubovsky E Malkin K Tucker MC Dubois JD Cohen WR Ballou DG Heppner Jr, Vaccine 28 5135 5144 10.1016/j.vaccine.2009.08.046 19737527
14. A liver-stage-specific antigen of Plasmodium falciparum characterized by gene cloning. C Guerin-Marchand P Druilhe B Galey A Londono J Patarapotikul RL Beaudoin C Dubeaux A Tartar O Mercereau-Puijalon G Langsley, Nature 1987 329 164 167 10.1038/329164a0 3306406 (Pubitemid 17125254)
15. Protection against Plasmodium falciparum malaria in chimpanzees by immunization with the conserved pre-erythrocytic liver-stage antigen 3. P Daubersies AW Thomas P Millet K Brahimi JA Langermans B Ollomo L BenMohamed B Slierendregt W Eling A Van Belkum G Dubreuil JF Meis C Guérin-Marchand S Cayphas J Cohen H Gras-Masse P Druilhe, Nat Med 2000 6 1258 1263 10.1038/81366 11062538
16. Strain specificity in the liver-stage development of Plasmodium falciparum in primary cultures of new world monkey hepatocytes. P Millet CT Atkinson M Aikawa MR Hollingdale WE Collins, Am J Trop Med Hyg 1991 45 236 242 1877718
17. Establishment of a human hepatocyte line that supports in vitro development of the exo-erythrocytic stages of the malaria parasites Plasmodium falciparum and P. vivax. J Sattabongkot N Yimamnuaychoke S Leelaudomlipi M Rasameesoraj R Jenwithisuk RE Coleman R Udomsangpetch L Cui TG Brewer, Am J Trop Med Hyg 2006 74 708 715 16687667 (Pubitemid 46774383)
18. Structure of Plasmodium falciparum liver stage antigen-1. J Zhu MR Hollingdale, Mol Biochem Parasitol 1991 48 223 226 10.1016/0166-6851(91)90117-O 1840628
19. Plasmodium falciparum liver stage antigen-1 is well conserved and contains potent B and T cell determinants. DA Fidock H Gras-Masse JP Lepers K Brahimi L Benmohamed S Mellouk C Guerin-Marchand A Londono L Raharimalala JF Meis, J Immunol 1994 153 190 204 7515922 (Pubitemid 24186532)
20. Structural characteristics of immunogenic liver-stage antigens derived from P. falciparum malarial proteins. G Cifuentes M Vanegas NL Martinez C Pirajan ME Patarroyo, Biochem Biophys Res Commun 2009 384 455 460 10.1016/j.bbrc.2009.04.138 19422790
21. T lymphocytes from volunteers immunized with irradiated Plasmodium falciparum sporozoites recognize liver and blood stage malaria antigens. U Krzych JA Lyon T Jareed I Schneider MR Hollingdale DM Gordon WR Ballou, J Immunol 1995 155 4072 4077 7561118
22. Biology and immunology of sporozoite invasion of liver cells and exoerythrocytic development of malaria parasites. MR Hollingdale, Prog Allergy 1988 41 15 48 3043420
23. Fine structure of the malaria parasite Plasmodium falciparum in human hepatocytes in vitro. JF Meis PJ Rijntjes JP Verhave T Ponnudurai MR Hollingdale JE Smith RE Sinden PH Jap JH Meuwissen SH Yap, Cell Tissue Res 1986 244 345 350 10.1007/BF00219210 3521880 (Pubitemid 16053385)
24. In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei in a hepatoma cell line. MR Hollingdale P Leland AL Schwartz, Am J Trop Med Hyg 1983 32 4 682 684 6349397 (Pubitemid 13040990)
25. Ultrastructure of in vitro cultured exoerythrocytic stage of Plasmodium berghei in a hepatoma cell line. M Aikawa A Schwartz S Uni R Nussenzweig M Hollingdale, Am J Trop Med Hyg 1984 33 792 799 6091467 (Pubitemid 15201689)
26. Electron microscopy of Plasmodium vivax exoerythrocytic schizonts grown in vitro in a hepatoma cell line. S Uni M Aikawa WE Collins CC Campbell MR Hollingdale, Am J Trop Med Hyg 1985 34 1017 1021 3010750 (Pubitemid 16204437)
27. Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. K Baer C Klotz SH Kappe T Schnieder U Frevert, PLoS Pathog 2007 3 171 10.1371/journal.ppat.0030171 17997605
28. Exoerythrocytic merozoites of Plasmodium berghei in rat hepatic Kupffer cells. JA Terzakis JP Vanderberg D Foley S Shustak, J Protozool 1979 26 385 389 395294 (Pubitemid 10188426)
29. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. A Sturm R Amino C van de Sand T Regen S Retzlaff A Rennenberg A Krueger JM Pollok R Menard VT Heussler, Science 2006 313 1287 1290 10.1126/science.1129720 16888102 (Pubitemid 44330952)
30. Live and let die: manipulation of host hepatocytes by exoerythrocytic Plasmodium parasites. A Sturm V Heussler, Med Microbiol Immunol 2007 196 127 133 10.1007/s00430-007-0044-3 17410380 (Pubitemid 47300256)
31. Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. D Aeschlimann V Thomazy, Connect Tissue Res 2000 41 1 27 10.3109/03008200009005638 10826705 (Pubitemid 30246155)
32. Apoptosis: molecular mechanisms in programmed cell death. L Fesus PJ Davies M Piacentini, Eur J Cell Biol 1991 56 170 177 1802705
33. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. H Nakaoka DM Perez KJ Baek T Das A Husain K Misono MJ Im RM Graham, Science 1994 264 1593 1596 10.1126/science.7911253 7911253
34. Tissue transglutaminase: a candidate effector element of physiological cell death. M Piacentini, Curr Top Microbiol Immunol 1995 200 163 175 7634831
35. Transglutaminase-mediated processing of fibronectin by endothelial cell monolayers. J Martinez DG Chalupowicz RK Roush A Sheth C Barsigian, Biochemistry 1994 33 2538 2545 10.1021/bi00175a024 7906954 (Pubitemid 24099661)
36. A role for tissue transglutaminase in hepatic injury and fibrogenesis, and its regulation by NF-kappaB. A Mirza SL Liu E Frizell J Zhu S Maddukuri J Martinez P Davies R Schwarting P Norton MA Zern, Am J Physiol 1997 272 2 Pt 1 281 288 9124352
37. Transglutaminase type II plays a protective role in hepatic injury. R Nardacci O Lo Iacono F Ciccosanti L Falasca M Addesso A Amendola G Antonucci A Craxi GM Fimia V Iadevaia G Melino L Ruco G Tocci G Ippolito M Piacentini, Am J Pathol 2003 162 1293 1303 12651621 (Pubitemid 36350673)
38. 'Tissue' transglutaminase release from apoptotic cells into extracellular matrix during human liver fibrogenesis. M Piacentini MG Farrace C Hassan B Serafini F Autuori, J Pathol 1999 189 92 98 10.1002/(SICI)1096-9896(199909)189: 1<92::AID-PATH386>3.0.CO;2-B 10451494 (Pubitemid 29406825)
39. High amount of epsilon-(gamma-glutamyl)lysine cross-links in Mallory bodies. K Zatloukal L Fesus H Denk E Tarcsa G Spurej G Bock, Lab Invest 1992 66 774 777 1351114
40. Hepatitis C virus replication in mice with chimeric human livers. DF Mercer DE Schiller JF Elliott DN Douglas C Hao A Rinfret WR Addison KP Fischer TA Churchill JR Lakey DL Tyrrell NM Kneteman, Nat Med 2001 7 927 933 10.1038/90968 11479625 (Pubitemid 32756430)
41. Plasmodium falciparum infection and exoerythrocytic development in mice with chimeric human livers. JB Sacci Jr U Alam D Douglas J Lewis DL Tyrrell AF Azad NM Kneteman, Int J Parasitol 2006 36 353 360 10.1016/j.ijpara.2005.10.014 16442544 (Pubitemid 43376117)
42. Assays for the measurement of tissue transglutaminase (type II) mediated protein crosslinking via epsilon-(gamma-glutamyl) lysine and N',N'-bis (gamma-glutamyl) polyamine linkages using biotin labelled casein. GR Lilley M Griffin PL Bonner, J Biochem Biophys Methods 1997 34 31 43 10.1016/S0165- 022X(96)01200-6 9089382 (Pubitemid 27113395)
43. Tissue transglutaminase and apoptosis: sense and antisense transfection studies with human neuroblastoma cells. G Melino M Annicchiarico-Petruzzelli L Piredda E Candi V Gentile PJ Davies M Piacentini, Mol Cell Biol 1994 14 6584 6596 7935379 (Pubitemid 24299727)
44. Rapid, large-scale isolation of Plasmodium berghei sporozoites from infected mosquitoes. ND Pacheco CP Strome F Mitchell MP Bawden RL Beaudoin, J Parasitol 1979 65 3 414 417 10.2307/3280286 39127 (Pubitemid 10222998)
45. JC Gerber, Guide for the care and use of laboratory animals National Academies Pressl, Washington 2010
46. Involucrin acts as a transglutaminase substrate at multiple sites. Y Etoh M Simon H Green, Biochem Biophys Res Commun 1986 136 51 56 10.1016/0006- 291X(86)90875-2 2871834 (Pubitemid 16046694)
47. Two adjacent N-terminal glutamines of BM-40 (osteonectin, SPARC) act as amine acceptor sites in transglutaminaseC-catalyzed modification. C Hohenadl K Mann U Mayer R Timpl M Paulsson D Aeschlimann, J Biol Chem 1995 270 23415 23420 10.1074/jbc.270.40.23415 7559501
48. Amine binding sites in acyl intermediates of transglutaminases. Human blood plasma enzyme (activated coagulation factor XIII) and guinea pig liver enzyme. M Gross NK Whetzel JE Folk, J Biol Chem 1977 252 3752 3759 16916 (Pubitemid 8116112)
49. Structural features of glutamine substrates for transglutaminases. Role of extended interactions in the specificity of human plasma factor XIIIa and of the guinea pig liver enzyme. JJ Gorman JE Folk, J Biol Chem 1984 259 9007 9010 6146608 (Pubitemid 14098877)
50. Full-chain Protein Structure Prediction Server. Robetta, http://robetta.bakerlab.org
51. Automated prediction of CASP-5 structures using the Robetta server. D Chivian DE Kim L Malmstrom P Bradley T Robertson P Murphy CE Strauss R Bonneau CA Rohl D Baker, Proteins 2003 53 Suppl 6 524 533 10.1002/prot.10529 14579342 (Pubitemid 37352212)
52. Determinants of substrate specificity for factor XIII. J McDonagh H Fukue, Semin Thromb Hemost 1996 22 369 376 10.1055/s-2007-999034 8989819 (Pubitemid 27050705)
53. Migration of Plasmodium sporozoites through cells before infection. MM Mota G Pradel JP Vanderberg JC Hafalla U Frevert RS Nussenzweig V Nussenzweig A Rodriguez, Science 2001 291 141 144 10.1126/science.291.5501.141 11141568 (Pubitemid 32056684)
54. Retinoic acid-induced modulation of rat liver transglutaminase and total polyamines in vivo. M Piacentini L Fesus C Sartori MP Ceru, Biochem J 1988 253 33 38 2901832
55. Transglutaminase in Plasmodium parasites: activity and putative role in oocysts and blood stages. A Adini M Krugliak H Ginsburg L Li L Lavie A Warburg, Mol Biochem Parasitol 2001 117 161 168 10.1016/S0166-6851(01)00345-0 11606226 (Pubitemid 32972277)
56. A Plasmodium whole-genome synteny map: indels and synteny breakpoints as foci for species-specific genes. TW Kooij JM Carlton SL Bidwell N Hall J Ramesar CJ Janse AP Waters, PLoS Pathog 2005 1 44 10.1371/journal.ppat.0010044 16389297
57. HGF/MET signalling protects Plasmodium-infected host cells from apoptosis. P Leiriao SS Albuquerque S Corso GJ van Gemert RW Sauerwein A Rodriguez S Giordano MM Mota, Cell Microbiol 2005 7 603 609 10.1111/j.1462-5822. 2004.00490.x 15760460 (Pubitemid 40439458)