Evolutionary relationships and protein domain architecture in an expanded calpain superfamily in kinetoplastid parasites

Journal of Molecular Evolution

Volumn 61, Issue 6, 2005, Pages 742-757

  Ersfeld, Klaus ^a   Barraclough, Helen ^b,d   Gull, Keith ^c  

^a UNIVERSITY OF HULL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d ST VINCENT S HOSPITAL   (Australia)

Author keywords

Acylation; Calpain; Cytoskeleton; Genome; Leishmania; Microtubules; Multigene family; Parasites; Protein domains; Trypanosoma

Indexed keywords

CALPAIN; CELL MEMBRANE PROTEIN; FATTY ACID; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTOZOAL PROTEIN;

ACYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; FLAGELLATE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC CONSERVATION; GENOME ANALYSIS; LEISHMANIA MAJOR; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTOZOAL GENETICS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CALPAIN; DATABASES, PROTEIN; EVOLUTION, MOLECULAR; LEISHMANIA MAJOR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA CRUZI;

EUKARYOTA; KINETOPLASTIDA; LEISHMANIA MAJOR; MAMMALIA; MASTIGOPHORA (FLAGELLATES); TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

EID: 28244461606     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-004-0272-8     Document Type: Article

References (64)

1. Barnes TM, Hodgkin J (1996) The tra-3 sex determination gene of Caenorhabditis elegans encodes a member of the calpain regulatory protease family. EMBO J 15:4477-4484
2. Bartlett GJ, Borkakoti N, Thornton JM (2003) Catalysing new reactions during evolution: economy of residues and mechanism. J Mol Biol 331:829-860
3. Berti PJ, Storer AC (1995) Alignment/phylogeny of the papain superfamily of cysteine proteases. J Mol Biol 246:273-283
4. Beverley SM (2003) Protozomics: trypanosomatid parasite genetics comes of age. Nat Rev Genet 4:11-19
5. Bhatt A, Kaverina I, Otey C, Huttenlocher A (2002) Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J Cell Sci 115:3415-3425
6. Bourgeau G, Lapointe H, Peloquin P, Mayrand D (1992) Cloning, expression, and sequencing of a protease gene (tpr) from Porphyromonas gingivalis W83 in Escherichia coli. Infect Immun 60:3186-3192
7. Boutin JA (1997) Myristoylation. Cell Signal 9:15-35
8. Bringaud F, Vedrenne C, Cuvillier A, Parzy D, Baltz D, Tetaud E, Pays E, Venegas J, Merlin G, Baltz T (1998) Conserved organization of genes in trypanosomatids. Mol Biochem Parasitol 94:249-264
9. Burn P, Burger MM (1987) The cytoskeletal protein vinculin contains transformation-sensitive, covalently bound lipid. Science 235:476-479
10. Cox FEG, Kreier JP, Wakelin D (1998) Parasitology. In: Collier L, Balows A, Sussman M (eds) Topley & Wilson's microbiology and microbial infections. Arnold, London
11. de Meeus T, Renaud F (2002) Parasites within the new phylogeny of eukaryotes. Trends Parasitol 18:247-251
12. Dear N, Matena K, Vingron M, Boehm T (1997) A new subfamily of vertebrate calpains lacking a calmodulin-like domain: implications for calpain regulation and evolution. Genomics 45:175-184
13. Dear TN, Boehm T (1999) Diverse mRNA expression patterns of the mouse calpain genes Capn5, Capn6 and Capn11 during development. Mech Dev 89:201-209
14. Denison SH, Orejas M, Arst HN Jr (1995) Signaling of ambient pH in Aspergillus involves a cysteine protease. J Biol Chem 270:28519-28522
15. Devedjiev Y, Popov A, Atanasov B, Bartunik HD (1997) X-ray structure at 1.76 A resolution of a polypeptide phospholipase A2 inhibitor. J Mol Biol 266:160-172
16. Diviani D, Scott JD (2001) AKAP signaling complexes at the cytoskeleton. J Cell Sci 114:1431-1437
17. El-Sayed NM, Hegde P, Quackenbush J, Melville SE, Donelson JE (2000) The African trypanosome genome. Int J Parasitol 30:329-345
18. El-Sayed NM, Ghedin E, Song J, MacLeod A, Bringaud F, Larkin C, Wanless D, Peterson J, Hou L, Taylor S, Tweedie A, Biteau N, Khalak HG, Lin X, Mason T, Hannick L, Caler E, Blandin G, Bartholomeu D, Simpson AJ, Kaul S, Zhao H, Pai G, Van Aken S, Utterback T, Haas B, Koo HL, Umayam L, Suh B, Gerrard C, Leech V, Qi R, Zhou S, Schwartz D, Feldblyum T, Salzberg S, Tait A, Turner CM, Ullu E, White O, Melville S, Adams MD, Fraser CM, Donelson JE (2003) The sequence and analysis of Trypanosoma brucei chromosome II. Nucleic Acids Res 31:4856-4863
19. Emori Y, Ohno S, Tobita M, Suzuki K (1986) Gene structure of calcium-dependent protease retains the ancestral organization of the calcium-binding protein gene. FEBS Lett 194:249-252
20. Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83:731-801
21. Gull K (1999) The cytoskeleton of trypanosomatid parasites. Annu Rev Microbiol 53:629-655
22. Hall N, Berriman M, Lennard NJ, Harris BR, Hertz-Fowler C, Bart-Delabesse EN, Gerrard CS, Atkin RJ, Barron AJ, Bowman S, Bray-Allen SP, Bringaud F, Clark LN, Corton CH, Cronin A, Davies R, Doggett J, Fraser A, Gruter E, Hall S, Harper AD, Kay MP, Leech V, Mayes R, Price C, Quail MA, Rabbinowitsch E, Reitter C, Rutherford K, Sasse J, Sharp S, Shownkeen R, MacLeod A, Taylor S, Tweedie A, Turner CM, Tait A, Gull K, Barrell B, Melville SE (2003) The DNA sequence of chromosome I of an African trypanosome: gene content, chromosome organisation, recombination and polymorphism. Nucleic Acids Res 31:4864-4873
23. Hertz-Fowler C, Ersfeld K, Gull K (2001) CAP5.5, a life-cycle-regulated, cytoskeleton-associated protein is a member of a novel family of calpain-related proteins in Trypanosoma brucei. Mol Biochem Parasitol 116:25-34
24. Horikawa Y, Oda N, Cox NJ, Li X, Orho-Melander M, Hara M, Hinokio Y, Lindner TH, Mashima H, Schwarz PE, del Bosque-Plata L , Oda Y, Yoshiuchi I, Colilla S, Polonsky KS, Wei S, Concannon P, Iwasaki N, Schulze J, Baier LJ, Bogardus C, Groop L, Boerwinkle E, Hanis CL, Bell GI (2000) Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nat Genet 26:163-175
25. Hosfield CM, Elce JS, Davies PL, Jia Z (1999a) Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J 18:6880-6889
26. Hosfield CM, Ye Q, Arthur JS, Hegadorn C, Croall DE, Elce JS, Jia Z (1999b) Crystallization and X-ray crystallographic analysis of m-calpain, a Ca2+-dependent protease. Acta Crystallogr D Biol Crystallogr 55(8):1484-1846
27. Huang Y, Wang KK (2001) The calpain family and human disease. Trends Mol Med 7:355-362
28. Jekely G, Friedrich P (1999) The evolution of the calpain family as reflected in paralogous chromosome regions. J Mol Evol 49:272-281
29. Lafaille JJ, Linss J, Krieger MA, Souto-Padron T, de Souza W, Goldenberg S (1989) Structure and expression of two Trypanosoma cruzi genes encoding antigenic proteins bearing repetitive epitopes. Mol Biochem Parasitol 35:127-136
30. Lamb AL, Torres AS, O'Halloran TV, Rosenzweig AC (2000) Heterodimer formation between superoxide dismutase and its copper chaperone. Biochemistry 39:14720-14727
31. Maretzki D, Mariani M, Lutz HU (1990) Fatty acid acylation of membrane skeletal proteins in human erythrocytes. FEBS Lett 259:305-310
32. Margis R, Margis-Pinheiro M (2003) Phytocalpains: orthologous calcium-dependent cysteine proteinases. Trends Plant Sci 8:58-62
33. Mariani M, Maretzki D, Lutz HU (1993) A tightly membrane-associated subpopulation of spectrin is 3H-palmitoylated. J Biol Chem 268:12996-13001
34. Matthews KR, Gull K (1994) Evidence for an interplay between cell cycle progression and the initiation of differentiation between life cycle forms of African trypanosomes. J Cell Biol 125:1147-1156
35. Maurer-Stroh S, Eisenhaber B, Eisenhaber F (2002) N-terminal N-myristoylation of proteins: prediction of substrate proteins from amino acid sequence. J Mol Biol 317:541-557
36. Moldoveanu T, Hosfield CM, Lim D, Elce JS, Jia Z, Davies PL (2002) A Ca(2+) switch aligns the active site of calpain. Cell 108:649-660
37. Moldoveanu T, Jia Z, Davies PL (2004) Calpain activation by cooperative Ca2+ binding at two non-EF-hand sites. J Biol Chem 279:6106-6114
38. Mottram JC, Helms MJ, Coombs GH, Sajid M (2003) Clan CD cysteine peptidases of parasitic protozoa. Trends Parasitol 19:182-187
39. Muller N, Hemphill A, Imboden M, Duvallet G, Dwinger RH, Seebeck T (1992) Identification and characterization of two repetitive non-variable antigens from African trypanosomes which are recognized early during infection. Parasitology 104(1):111-120
40. Myler PJ, Audleman L, deVos T, Hixson G, Kiser P, Lemley C, Magness C, Rickel E, Sisk E, Sunkin S, Swartzell S, Westlake T, Bastien P, Fu G, Ivens A, Stuart K (1999) Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes. Proc Natl Acad Sci USA 96:2902-2906
41. Newlon MG, Roy M, Morikis D, Hausken ZE, Coghlan V, Scott JD, Jennings PA (1999) The molecular basis for protein kinase A anchoring revealed by solution NMR. Nat Struct Biol 6:222-227
42. Newlon MG, Roy M, Morikis D, Carr DW, Westphal R, Scott JD, Jennings PA (2001) A novel mechanism of PKA anchoring revealed by solution structures of anchoring complexes. EMBO J 20:1651-1662
43. Ohno S, Emori Y, Imajoh S, Kawasaki H, Kisaragi M, Suzuki K (1984) Evolutionary origin of a calcium-dependent protease by fusion of genes for a thiol protease and a calcium-binding protein? Nature 312:566-570
44. Ono Y, Sorimachi H, Suzuki K (1998) Structure and physiology of calpain, an enigmatic protease. Biochem Biophys Res Commun 245:289-294
45. Pils B, Schultz J (2004) Inactive enzyme-homologues find new function in regulatory processes. J Mol Biol 340:399-404
46. Resh MD (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451:1-16
47. Reverter D, Strobl S, Fernandez-Catalan C, Sorimachi H, Suzuki K, Bode W (2001) Structural basis for possible calcium-induced activation mechanisms of calpains. Biol Chem 382:753-766
48. Richard I, Broux O, Allamand V, et al. (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81:27-40
49. Rizo J, Sudhof TC (1998) C2-domains, structure and function of a universal Ca2+-binding domain. J Biol Chem 273:15879-15882
50. Sajid M, McKerrow JH (2002) Cysteine proteases of parasitic organisms. Mol Biochem Parasitol 120:1-21
51. Sato K, Kawashima S (2001) Calpain function in the modulation of signal transduction molecules. Biol Chem 382:743-751
52. Saxena A, Worthey EA, Yan S, Leland A, Stuart KD, Myler PJ (2003) Evaluation of differential gene expression in Leishmania major Friedlin procyclics and metacyclics using DNA microarray analysis. Mol Biochem Parasitol 129:103-114
53. Sorimachi H, Suzuki K (2001) The structure of calpain. J Biochem (Tokyo) 129:653-664
54. Sorimachi H, Ishiura S, Suzuki K (1997) Structure and physiological function of calpains. Biochem J 328(3):721-732
55. Staufenbiel M, Lazarides E (1986) Ankyrin is fatty acid acylated in erythrocytes. Proc Natl Acad Sci USA 83:318-322
56. Stevens JR, Noyes HA, Dover GA, Gibson WC (1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118(1):107-116
57. Strobl S, Fernandez-Catalan C, Braun M, Huber R, Masumoto H, Nakagawa K, Irie A, Sorimachi H, Bourenkow G, Bartunik H, Suzuki K, Bode W (2000) The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc Natl Acad Sci USA 97:588-592
58. Taveau M, Bourg N, Sillon G, Roudaut C, Bartoli M, Richard I (2003) Calpain 3 is activated through autolysis within the active site and lyzes sarcomeric and sarcolemmal components. Mol Cell Biol 23:9127-9135
59. Todd AE, Orengo CA, Thornton JM (2001) Evolution of function in protein superfamilies, from a structural perspective. J Mol Biol 307:1113-1143
60. Todd AE, Orengo CA, Thornton JM (2002) Sequence and structural differences between enzyme and nonenzyme homologs. Structure (Cambr) 10:1435-1451
61. Tull D, Vince JE, Callaghan JM, Naderer T, Spurck T, McFadden GI, Currie G, Ferguson K, Bacic A, McConville MJ (2004) SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol Biol Cell 15:4775-4786
62. Wilson ME, Young BM, Andersen KP, Weinstock JV, Metwali A, Ali KM, Donelson JE (1995) A recombinant Leishmania chagasi antigen that stimulates cellular immune responses in infected mice. Infect Immun 63:2062-2069
63. Worthey EA, Martinez-Calvillo S, Schnaufer A, Aggarwal G, Cawthra J, Fazelinia G, Fong C, Fu G, Hassebrock M, Hixson G, Ivens AC, Kiser P, Marsolini F, Rickell E, Salavati R, Sisk E, Sunkin SM, Stuart KD, Myler PJ (2003) Leishmania major chromosome 3 contains two long convergent polycistronic gene clusters separated by a tRNA gene. Nucleic Acids Res 31:4201-4210
64. Wu Y, Wang X, Liu X, Wang Y (2003) Data-mining approaches reveal hidden families of proteases in the genome of malaria parasite. Genome Res 13:601-616