New insights into parasite rhomboid proteases

Molecular and Biochemical Parasitology

Volumn 182, Issue 1-2, 2012, Pages 27-36

  Santos, Joana M ^a,b   Graindorge, Arnault ^a   Soldati Favre, Dominique ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

Apicomplexa; Intramembrane cleavage; Invasion; Kinetoplastida; Pathogenesis; Phagocytosis; Protozoan; Replication; Rhomboid protease; Signalling

Indexed keywords

MICRONEMAL PROTEIN PROTEASE 1; PROTEINASE; RHOMBOID PROTEASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; APICOMPLEXA; ARTICLE; CELL ADHESION; DROSOPHILA MELANOGASTER; ENTAMOEBA HISTOLYTICA; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; KINETOPLASTIDA; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTOZOON; SIGNAL TRANSDUCTION; TOXOPLASMA GONDII;

ANIMALS; APICOMPLEXA; CATALYTIC DOMAIN; CELL MEMBRANE; ENZYME ACTIVATION; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PEPTIDE HYDROLASES; PHYLOGENY; PROTOZOAN PROTEINS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

APICOMPLEXA; ENTAMOEBA HISTOLYTICA; KINETOPLASTIDA; PROTOZOA; TOXOPLASMA GONDII;

EID: 84856752480     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2011.11.010     Document Type: Article

References (76)

1. E. Erez, D. Fass, and E. Bibi How intramembrane proteases bury hydrolytic reactions in the membrane Nature 459 7245 2009 371 378
2. J.R. Lee, S. Urban, C.F. Garvey, and M. Freeman Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila Cell 107 2 2001 161 171 (Pubitemid 33035943)
3. S. Urban, J.R. Lee, and M. Freeman Drosophila Rhomboid-1 defines a family of putative intramembrane serine proteases Cell 107 2 2001 173 182 (Pubitemid 33035944)
4. E.V. Koonin, K.S. Makarova, I.B. Rogozin, L. Davidovic, M.C. Letellier, and L. Pellegrini The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers Genome Biol 4 3 2003 R19
5. M.K. Lemberg, and M. Freeman Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases Genome Res 17 11 2007 1634 1646 (Pubitemid 350074859)
6. S. Urban, and R.P. Baker In vivo analysis reveals substrate-gating mutants of a rhomboid intramembrane protease display increased activity in living cells Biol Chem 389 8 2008 1107 1115
7. E.J. Greenblatt, J.A. Olzmann, and R.R. Kopito Derlin-1 is a rhomboid pseudoprotease required for the dislocation of mutant alpha-1 antitrypsin from the endoplasmic reticulum Nat Struct Mol Biol 18 10 2011 1147 1152
8. M.E. Kirst, D.J. Meyer, B.C. Gibbon, R. Jung, and R.S. Boston Identification and characterization of endoplasmic reticulum-associated degradation proteins differentially affected by endoplasmic reticulum stress Plant Physiol 138 1 2005 218 231 (Pubitemid 43138122)
9. M. Zettl, C. Adrain, K. Strisovsky, V. Lastun, and M. Freeman Rhomboid family pseudoproteases use the ER quality control machinery to regulate intercellular signaling Cell 145 1 2011 79 91
10. R. Tsruya, A. Wojtalla, S. Carmon, S. Yogev, A. Reich, and E. Bibi Rhomboid cleaves Star to regulate the levels of secreted Spitz EMBO J 26 5 2007 1211 1220 (Pubitemid 46398704)
11. K. Strisovsky, H.J. Sharpe, and M. Freeman Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates Mol Cell 36 6 2009 1048 1059
12. C. Adrain, K. Strisovsky, M. Zettl, L. Hu, M.K. Lemberg, and M. Freeman Mammalian EGF receptor activation by the rhomboid protease RHBDL2 EMBO Rep 12 5 2011 421 427
13. S. Maegawa, K. Koide, K. Ito, and Y. Akiyama The intramembrane active site of GlpG: an E. coli rhomboid protease, is accessible to water and hydrolyses an extramembrane peptide bond of substrates Mol Microbiol 64 2 2007 435 447 (Pubitemid 46632636)
14. C. Lazareno-Saez, C.L. Brooks, and M.J. Lemieux Structural comparison of substrate entry gate for rhomboid intramembrane peptidases Biochem Cell Biol Biochim Biol Cell 89 2 2011 216 223
15. S. Urban, D. Schlieper, and M. Freeman Conservation of intramembrane proteolytic activity and substrate specificity in prokaryotic and eukaryotic rhomboids Curr Biol 12 17 2002 1507 1512 (Pubitemid 35036649)
16. S. Urban, and M. Freeman Substrate specificity of rhomboid intramembrane proteases is governed by helix-breaking residues in the substrate transmembrane domain Mol Cell 11 6 2003 1425 1434 (Pubitemid 36776530)
17. Y. Akiyama, and S. Maegawa Sequence features of substrates required for cleavage by GlpG: an Escherichia coli rhomboid protease Mol Microbiol 64 4 2007 1028 1037 (Pubitemid 46743969)
18. E. Erez, and E. Bibi Cleavage of a multispanning membrane protein by an intramembrane serine protease Biochemistry 48 51 2009 12314 12322
19. O. Lohi, S. Urban, and M. Freeman Diverse substrate recognition mechanisms for rhomboids; thrombomodulin is cleaved by Mammalian rhomboids Curr Biol 14 3 2004 236 241 (Pubitemid 38215352)
20. A. Schafer, M. Zick, J. Kief, M. Steger, H. Heide, and S. Duvezin-Caubet Intramembrane proteolysis of Mgm1 by the mitochondrial rhomboid protease is highly promiscuous regarding the sequence of the cleaved hydrophobic segment J Mol Biol 401 2 2010 182 193
21. M.K. Lemberg, J. Menendez, A. Misik, M. Garcia, C.M. Koth, and M. Freeman Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases EMBO J 24 3 2005 464 472 (Pubitemid 40343249)
22. S. Urban, and M.S. Wolfe Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity Proc Natl Acad Sci USA 102 6 2005 1883 1888 (Pubitemid 40261981)
23. M. Freeman Rhomboids: 7 years of a new protease family Semin Cell Dev Biol 20 2 2009 231 239
24. X. Lei, and Y.M. Li The processing of human rhomboid intramembrane serine protease RHBDL2 is required for its proteolytic activity J Mol Biol 394 5 2009 815 825
25. A.R. Sherratt, M.V. Braganza, E. Nguyen, T. Ducat, and N.K. Goto Insights into the effect of detergents on the full-length rhomboid protease from Pseudomonas aeruginosa and its cytosolic domain Biochim Biophys Acta 1788 11 2009 2444 2453
26. T. Rousso, J. Lynch, S. Yogev, S. Roth, E.D. Schejter, and B.Z. Shilo Generation of distinct signaling modes via diversification of the Egfr ligand-processing cassette Development 137 20 2010 3427 3437
27. M.V. Sundaram Vulval development: the battle between Ras and Notch Curr Biol 14 8 2004 R311 R313
28. A. Dutt, S. Canevascini, E. Froehli-Hoier, and A. Hajnal EGF signal propagation during C. elegans vulval development mediated by ROM-1 rhomboid PLoS Biol 2 11 2004 e334
29. J.C. Pascall, and K.D. Brown Intramembrane cleavage of ephrinB3 by the human rhomboid family protease: RHBDL2 Biochem Biophys Res Commun 317 1 2004 244 252 (Pubitemid 38401991)
30. M. Gallio, G. Sturgill, P. Rather, and P. Kylsten A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes Proc Natl Acad Sci USA 99 19 2002 12208 12213
31. L.G. Stevenson, K. Strisovsky, K.M. Clemmer, S. Bhatt, M. Freeman, and P.N. Rather Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase Proc Natl Acad Sci USA 104 3 2007 1003 1008 (Pubitemid 46154726)
32. S. Urban Making the cut: central roles of intramembrane proteolysis in pathogenic microorganisms Nat Rev Microbiol 7 6 2009 411 423
33. R.B. Hill, and L. Pellegrini The PARL family of mitochondrial rhomboid proteases Semin Cell Dev Biol 21 6 2010 582 592
34. A.J. Whitworth, J.R. Lee, V.M. Ho, R. Flick, R. Chowdhury, and G.A. McQuibban Rhomboid-7 and HtrA2/Omi act in a common pathway with the Parkinson's disease factors Pink1 and Parkin Dis Models Mech 1 2-3 2008 168 174 discussion 173
35. E. Deas, H. Plun-Favreau, S. Gandhi, H. Desmond, S. Kjaer, and S.H. Loh PINK1 cleavage at position A103 by the mitochondrial protease PARL Hum Mol Genet 20 5 2011 867 879
36. S.M. Jin, M. Lazarou, C. Wang, L.A. Kane, D.P. Narendra, and R.J. Youle Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL J Cell Biol 191 5 2010 933 942
37. G. Shi, J.R. Lee, D.A. Grimes, L. Racacho, D. Ye, and H. Yang Functional alteration of PARL contributes to mitochondrial dysregulation in Parkinson's disease Hum Mol Genet 20 10 2011 1966 1974
38. S. Cipolat, T. Rudka, D. Hartmann, V. Costa, L. Serneels, and K. Craessaerts Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling Cell 126 1 2006 163 175
39. S. Duvezin-Caubet, M. Koppen, J. Wagener, M. Zick, L. Israel, and A. Bernacchia OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria Mol Biol Cell 18 9 2007 3582 3590 (Pubitemid 47378695)
40. M.M. Kanaoka, S. Urban, M. Freeman, and K. Okada An Arabidopsis Rhomboid homolog is an intramembrane protease in plants FEBS Lett 579 25 2005 5723 5728 (Pubitemid 41455654)
41. K. Karakasis, D. Taylor, and K. Ko Uncovering a link between a plastid translocon component and rhomboid proteases using yeast mitochondria-based assays Plant Cell Physiol 48 4 2007 655 661 (Pubitemid 47356111)
42. T.J. Dowse, and D. Soldati Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature Trends Parasitol 21 6 2005 254 258 (Pubitemid 40726312)
43. V.B. Carruthers, P.A. Cotter, and C.A. Kumamoto Microbial pathogenesis: mechanisms of infectious disease Cell Host Microbe 2 4 2007 214 219 (Pubitemid 47500825)
44. F. Brossier, T.J. Jewett, J.L. Lovett, and L.D. Sibley C-terminal processing of the Toxoplasma protein MIC2 is essential for invasion into host cells J Biol Chem 278 8 2003 6229 6234 (Pubitemid 36800878)
45. S.A. Howell, F. Hackett, A.M. Jongco, C. Withers-Martinez, K. Kim, and V.B. Carruthers Distinct mechanisms govern proteolytic shedding of a key invasion protein in Apicomplexan pathogens Mol Microbiol 57 5 2005 1342 1356 (Pubitemid 41176527)
46. C. Opitz, M. Di Cristina, M. Reiss, T. Ruppert, A. Crisanti, and D. Soldati Intramembrane cleavage of microneme proteins at the surface of the Apicomplexan parasite Toxoplasma gondii EMBO J 21 7 2002 1577 1585 (Pubitemid 34614614)
47. X.W. Zhou, M.J. Blackman, S.A. Howell, and V.B. Carruthers Proteomic analysis of cleavage events reveals a dynamic two-step mechanism for proteolysis of a key parasite adhesive complex Mol Cell Proteomics 3 6 2004 565 576 (Pubitemid 38878516)
48. R.A. O'Donnell, F. Hackett, S.A. Howell, M. Treeck, N. Struck, and Z. Krnajski Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite J Cell Biol 174 7 2006 1023 1033
49. T. Triglia, W.H. Tham, A. Hodder, and A.F. Cowman Reticulocyte binding protein homologues are key adhesins during erythrocyte invasion by Plasmodium falciparum Cell Microbiol 11 11 2009 1671 1687
50. R.P. Baker, R. Wijetilaka, and S. Urban Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria PLoS Pathog 2 10 2006 e113
51. A.F. Cowman, and B.S. Crabb Invasion of red blood cells by malaria parasites Cell 124 4 2006 755 766 (Pubitemid 43261450)
52. F. Brossier, T.J. Jewett, L.D. Sibley, and S. Urban A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma Proc Natl Acad Sci USA 102 11 2005 4146 4151 (Pubitemid 40388570)
53. T.J. Dowse, J.C. Pascall, K.D. Brown, and D. Soldati Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion Int J Parasitol 35 7 2005 747 756 (Pubitemid 40733613)
54. S. Singh, M. Plassmeyer, D. Gaur, and L.H. Miller Mononeme: a new secretory organelle in Plasmodium falciparum merozoites identified by localization of Rhomboid-1 protease Proc Natl Acad Sci USA 104 50 2007 20043 20048
55. F. Brossier, G.L. Starnes, W.L. Beatty, and L.D. Sibley Microneme rhomboid protease TgROM1 is required for efficient intracellular growth of Toxoplasma gondii Eukaryot Cell 7 4 2008 664 674 (Pubitemid 351959901)
56. P. Srinivasan, I. Coppens, and M. Jacobs-Lorena Distinct roles of Plasmodium Rhomboid 1 in parasite development and malaria pathogenesis PLoS Pathog 5 1 2009 e1000262
57. I.M. Vera, W.L. Beatty, P. Sinnis, and K. Kim Plasmodium protease ROM1 is important for proper formation of the parasitophorous vacuole PLoS Pathog 7 9 2011 e1002197
58. L. Sheiner, T.J. Dowse, and D. Soldati-Favre Identification of trafficking determinants for polytopic rhomboid proteases in Toxoplasma gondii Traffic 9 5 2008 665 677 (Pubitemid 351494299)
59. M. Nishi, K. Hu, J.M. Murray, and D.S. Roos Organellar dynamics during the cell cycle of Toxoplasma gondii J Cell Sci 121 Pt 9 2008 1559 1568 (Pubitemid 351936320)
60. J.S. Buguliskis, F. Brossier, J. Shuman, and L.D. Sibley Rhomboid 4 (ROM4) affects the processing of surface adhesins and facilitates host cell invasion by Toxoplasma gondii PLoS Pathog 6 4 2010 e1000858
61. J.M. Santos, D.J. Ferguson, M.J. Blackman, and D. Soldati-Favre Intramembrane cleavage of AMA1 triggers Toxoplasma to switch from an invasive to a replicative mode Science 331 6016 2011 473 477
62. J. Mital, M. Meissner, D. Soldati, and G.E. Ward Conditional expression of Toxoplasma gondii apical membrane antigen-1 (TgAMA1) demonstrates that TgAMA1 plays a critical role in host cell invasion Mol Biol Cell 16 9 2005 4341 4349 (Pubitemid 41262901)
63. Anna Olivieri CRC, Fiona Hackett, Chrislaine Withers-Martinez, Joshua Marshall, Helen R. Flynn, J. Mark Skehel and Michael J. Blackman Juxtamembrane shedding of Plasmodium falciparum apical membrane antigen-1 is non-sequence dependent and essential, and aids evasion of invasion-inhibitory antibodies. PLoS Pathog, in press.
64. H. Kessler, A. Herm-Götz, S. Hegge, M. Rauch, D. Soldati-Favre, and F. Frischknecht Microneme protein 8 - a new essential invasion factor in Toxoplasma gondii J Cell Sci 121 Pt 7 2008 947 956 (Pubitemid 351639414)
65. S. Singh, M.M. Alam, I. Pal-Bhowmick, J.A. Brzostowski, and C.E. Chitnis Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites PLoS Pathog 6 2 2010 e1000746
66. E. Trasarti, E. Pizzi, E. Pozio, and F. Tosini The immunological selection of recombinant peptides from Cryptosporidium parvum reveals 14 proteins expressed at the sporozoite stage: 7 of which are conserved in other apicomplexa Mol Biochem Parasitol 152 2 2007 159 169
67. G. Yang, J. Li, X. Zhang, Q. Zhao, Q. Liu, and P. Gong Eimeria tenella: construction of a recombinant fowlpox virus expressing rhomboid gene and its protective efficacy against homologous infection Exp Parasitol 119 1 2008 30 36
68. L.A. Baxt, R.P. Baker, U. Singh, and S. Urban An Entamoeba histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion Genes Dev 22 12 2008 1636 1646 (Pubitemid 351846843)
69. L.A. Baxt, E. Rastew, R. Bracha, D. Mirelman, and U. Singh Downregulation of an Entamoeba histolytica rhomboid protease reveals roles in regulating parasite adhesion and phagocytosis Eukaryot Cell 9 8 2010 1283 1293
70. C.A. Coss, J.A. Robledo, G.M. Ruiz, and G.R. Vasta Description of Perkinsus andrewsi n. sp. isolated from the Baltic clam (Macoma balthica) by characterization of the ribosomal RNA locus: and development of a species-specific PCR-based diagnostic assay J Eukaryot Microbiol 48 1 2001 52 61 (Pubitemid 32180369)
71. J.M. Carlton, R.P. Hirt, J.C. Silva, A.L. Delcher, M. Schatz, and Q. Zhao Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis Science 315 5809 2007 207 212 (Pubitemid 46166360)
72. H.G. Morrison, A.G. McArthur, F.D. Gillin, S.B. Aley, R.D. Adam, and G.J. Olsen Genomic minimalism in the early diverging intestinal parasite Giardia lamblia Science 317 5846 2007 1921 1926 (Pubitemid 47509437)
73. J. Baum, A.G. Maier, R.T. Good, K.M. Simpson, and A.F. Cowman Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions PLoS Pathog 1 4 2005 e37
74. B.A. Bergmans, and B. De Strooper Gamma-secretases: from cell biology to therapeutic strategies Lancet Neurol 9 2 2010 215 226
75. O.A. Pierrat, K. Strisovsky, Y. Christova, J. Large, K. Ansell, and N. Bouloc Monocyclic beta-lactams are selective: mechanism-based inhibitors of rhomboid intramembrane proteases ACS Chem Biol 6 4 2011 325 335
76. S. Urban Taking the plunge: integrating structural, enzymatic and computational insights into a unified model for membrane-immersed rhomboid proteolysis Biochem J 425 3 2010 501 512