Calcium binding proteins and calcium signaling in prokaryotes

Cell Calcium

Volumn 57, Issue 3, 2015, Pages 151-165

  Domínguez, Delfina C ^a   Guragain, Manita ^b   Patrauchan, Marianna ^b  

^a UNIVERSITY OF TEXAS AT EL PASO   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Bacterial Ca2+ binding motifs; Ca2+ homeostasis; Ca2+ signaling in bacteria; Prokaryotic Ca2+ transporters

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); BETA CRYSTALLIN; CALCIUM BINDING PROTEIN; CALCIUM CHANNEL; CALCIUM ION; GAMMA CRYSTALLIN; SODIUM CALCIUM EXCHANGE PROTEIN;

CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DIVISION; CELL FUNCTION; CELL MATURATION; CELL METABOLISM; CELL MOTILITY; CELLULAR SECRETION; CELLULAR STRESS RESPONSE; HOST PATHOGEN INTERACTION; INTRACELLULAR SIGNALING; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SEQUENCE ANALYSIS; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; PHYSIOLOGY; PROKARYOTIC CELL; PROTEIN SECONDARY STRUCTURE;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

ANIMALS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; HUMANS; PROKARYOTIC CELLS; PROTEIN STRUCTURE, SECONDARY;

EID: 84923922028     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.12.006     Document Type: Review

References (196)

1. Permyakov E.A., Kretsinger R.H. Cell signaling, beyond cytosolic calcium in eukaryotes. J. Inorg. Biochem. 2009, 103:77-86.
2. Ikura M., Osawa M., Ames J.B. The role of calcium-binding proteins in the control of transcription: structure to function. BioEssays 2002, 24:625-636.
3. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4:517-529.
4. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
5. Sanders D., Brownlee C., Harper J.F. Communicating with calcium. Plant Cell 1999, 11:691-706.
6. Campbell A.K. Intracellular Calcium, Its Universal Role as Regulator 1983, John Wiley & Sons, Chichester.
7. 2+ homeostasis: different molecules for different purposes?. Cell. Mol. Life Sci. 2012, 69:1077-1104.
8. Hashimoto K., Kudla J. Calcium decoding mechanisms in plants. Biochimie 2011, 93:2054-2059.
9. 2+ response. Mol. Microbiol. 1993, 8:1005-1010.
10. 2+ level rises with repellents and falls with attractants in Escherichia coli chemotaxis. Proc. Natl. Acad. Sci. U S A 1995, 92:10777-10781.
11. Sarkisova S., Patrauchan M.A., Berglund D., Nivens D.E., Franklin M.J. Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J. Bacteriol. 2005, 187:4327-4337.
12. 2+ signaling during heterocyst differentiation. J. Biol. Chem. 2011, 286:12381-12388.
13. Guragain M., Lenaburg D.L., Moore F.S., Reutlinger I., Patrauchan M.A. Calcium homeostasis in Pseudomonas aeruginosa requires multiple transporters and modulates swarming motility. Cell Calcium 2013, 54:350-361.
14. Rosch J.W., Sublett J., Gao G., Wang Y.D., Tuomanen E.I. Calcium efflux is essential for bacterial survival in the eukaryotic host. Mol. Microbiol. 2008, 70:435-444.
15. Herbaud M.L., Guiseppi A., Denizot F., Haiech J., Kilhoffer M.C. Calcium signalling in Bacillus subtilis. Biochim. Biophys. Acta 1998, 1448:212-226.
16. 2+ in Escherichia coli highlight two putative influx mechanisms in response to changes in extracellular calcium. Cell Calcium 1999, 25:265-274.
17. Torrecilla I., Leganes F., Bonilla I., Fernandez-Pinas F. Use of recombinant aequorin to study calcium homeostasis and monitor calcium transients in response to heat and cold shock in cyanobacterial. Plant Physiol. 2000, 123:161-175.
18. 2+ in Escherichia coli. FEBS Lett. 1991, 282:405-408.
19. Leganes F., Forchhammer K., Fernandez-Pinas F. Role of calcium in acclimation of the cyanobacterium Synechococcus elongatus PCC 7942 to nitrogen starvation. Microbiology 2009, 155:25-34.
20. 2+ channels. Cell Calcium 2007, 41:97-106.
21. Naseem R., Wann K.T., Holland I.B., Campbell A.K. ATP regulates calcium efflux and growth in E. coli. J. Mol. Biol. 2009, 391:42-56.
22. Oomes S.J., Jonker M.J., Wittink F.R., Hehenkamp J.O., Breit T.M., Brul S. The effect of calcium on the transcriptome of sporulating B. subtilis cells. Int. J. Food Microbiol. 2009, 133:234-242.
23. Bilecen K., Yildiz F.H. Identification of a calcium-controlled negative regulatory system affecting Vibrio cholerae biofilm formation. Environ. Microbiol. 2009, 11:2015-2029.
24. Dominguez D.C. Proteome analysis of B. subtilis in response to calcium. J. Anal. Bioanal. Tech. 2011, S6.
25. Patrauchan M.A., Sarkisova S.A., Franklin M.J. Strain-specific proteome responses of Pseudomonas aeruginosa to biofilm-associated growth and to calcium. Microbiology 2007, 153:3838-3851.
26. Gode-Potratz C.J., Chodur D.M., McCarter L.L. Calcium and iron regulate swarming and type III secretion in Vibrio parahaemolyticus. J. Bacteriol. 2010, 192:6025-6038.
27. Yang K. Prokaryotic calmodulins: recent developments and evolutionary implications. J. Mol. Microbiol. Biotechnol. 2001, 3:457-459.
28. Rigden D.J., Jedrzejas M.J., Moroz O.V., Galperin M.Y. Structural diversity of calcium-binding proteins in bacteria: single-handed EF-hands?. Trends Microbiol. 2003, 11:295-297.
29. Zhou Y., Yang W., Kirberger M., Lee H.W., Ayalasomayajula G., Yang J.J. Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins. Proteins 2006, 65:643-655.
30. Aravind P., Mishra A., Suman S.K., Jobby M.K., Sankaranarayanan R., Sharma Y. The betagamma-crystallin superfamily contains a universal motif for binding calcium. Biochemistry 2009, 48:12180-12190.
31. (2+) in bacteria: a role for EF-hand proteins?. Trends Microbiol. 2002, 10:87-93.
32. Bylsma N., Drakenberg T., Andersson I., Leadlay P.F., Forsen S. Prokaryotic calcium-binding protein of the calmodulin superfamily. Calcium binding to a Saccharopolyspora erythraea 20kDa protein. FEBS Lett. 1992, 299:44-47.
33. Swan D.G., Hale R.S., Dhillon N., Leadlay P.F. A bacterial calcium-binding protein homologous to calmodulin. Nature 1987, 329:84-85.
34. Welch R.A. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr. Top Microbiol. Immunol. 2001, 257:85-111.
35. Jobby M.K., Sharma Y. Calcium-binding crystallins from Yersinia pestis. Characterization of two single betagamma-crystallin domains of a putative exported protein. J. Biol. Chem. 2005, 280:1209-1216.
36. Jobby M.K., Sharma Y. Caulollins from Caulobacter crescentus, a pair of partially unstructured proteins of betagamma-crystallin superfamily, gain structure upon binding calcium. Biochemistry 2007, 46:12298-12307.
37. (2)+-binding modules: evidences from big domains of Leptospira immunoglobulin-like (Lig) proteins. PloS One 2010, 5:e14377.
38. Linhartova I., Bumba L., Masin J., Basler M., Osicka R., Kamanova J., Prochazkova K., Adkins I., Hejnova-Holubova J., Sadilkova L., Morova J., Sebo P. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol. Rev. 2010, 34:1076-1112.
39. 2+-binding motif of betagamma-crystallins. J. Biol. Chem. 2014, 289:10958-10966.
40. Dominguez D.C., Adams H., Hageman J.H. Immunocytochemical localization of a calmodulinlike protein in Bacillus subtilis cells. J. Bacteriol. 1999, 181:4605-4610.
41. Tossavainen H., Permi P., Annila A., Kilpelainen I., Drakenberg T. NMR solution structure of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea. Eur. J. Biochem. 2003, 270:2505-2512.
42. Zhao Y., Shi Y., Zhao W., Huang X., Wang D., Brown N., Brand J., Zhao J. CcbP, a calcium-binding protein from Anabaena sp. PCC 7120, provides evidence that calcium ions regulate heterocyst differentiation. Proc. Natl. Acad. Sci. U S A 2005, 102:5744-5748.
43. Zhao X., Pang H., Wang S., Zhou W., Yang K., Bartlam M. Structural basis for prokaryotic calcium-mediated regulation by a Streptomyces coelicolor calcium binding protein. Protein Cell 2010, 1:771-779.
44. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
45. Gilabert J.A. Cytoplasmic calcium buffering. Adv. Exp. Med. Biol. 2012, 740:483-498.
46. Gangola P., Rosen B.P. Maintenance of intracellular calcium in Escherichia coli. J. Biol. Chem. 1987, 262:12570-12574.
47. Sarkisova S.A., Lotlikar S.R., Guragain M., Kubat R., Cloud J., Franklin M.J., Patrauchan M.A. A Pseudomonas aeruginosa EF-hand protein, EfhP (PA4107), modulates stress responses and virulence at high calcium concentration. PloS One 2014, 9:e98985.
48. Dominguez D.C. Calcium signalling in bacteria. Mol. Microbiol. 2004, 54:291-297.
49. Notari L., Pepe I.M., Cugnoli C., Morelli A. Adenylate kinase activity in rod outer segments of bovine retina. Biochim. Biophys. Acta 2001, 1504:438-443.
50. 2+-mediated protein kinase-phosphatase pathway. Plant Mol. Biol. 1996, 30:381-385.
51. Kim H.K., Park W.S., Kang S.H., Warda M., Kim N., Ko J.H., Prince Ael B., Han J. Mitochondrial alterations in human gastric carcinoma cell line. Am. J. Physiol. Cell Physiol. 2007, 293:C761-C771.
52. Docampo R., Ulrich P., Moreno S.N.J. Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365:775-784.
53. +-pyrophosphatase of Rhodospirillum rubrum is predominantly located in polyphosphate-rich acidocalcisomes. J. Biol. Chem. 2004, 279:51193-51202.
54. Seufferheld M., Vieira M.C.F., Ruiz F.A., Rodrigues C.O., Moreno S.N.J., Docampo R. Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. J. Biol. Chem. 2003, 278:29971-29978.
55. Docampo R., Moreno S.N.J. Acidocalcisomes. Cell Calcium 2011, 50:113-119.
56. Docampo R., de Souza W., Miranda K., Rohloff P., Moreno S.N.J. Acidocalcisomes-conserved from bacteria to man. Nat. Rev. Microbiol. 2005, 3:251-261.
57. Graham L.L., Beveridge T.J., Nanninga N. Periplasmic space and the concept of the periplasm. Trends Biochem. Sci. 1991, 16:328-329.
58. Matias V.R.F., Beveridge T.J. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 2005, 56:240-251.
59. Matias V.R.F., Beveridge T.J. Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J. Bacteriol. 2006, 188:1011-1021.
60. Zuber B., Haenni M., Ribeiro T., Minnig K., Lopes F., Moreillon P., Dubochet J. Granular layer in the periplasmic space of gram-positive bacteria and fine structures of Enterococcus gallinarum and Streptococcus gordonii septa revealed by cryo-electron microscopy of vitreous sections. J. Bacteriol. 2006, 188:6652-6660.
61. Chang C.F., Shuman H., Somlyo A.P. Electron probe analysis, X-ray mapping, and electron energy-loss spectroscopy of calcium, magnesium, and monovalent ions in log-phase and in dividing Escherichia coli B cells. J. Bacteriol. 1986, 167:935-939.
62. (2+) between the periplasm and the cytosol of Escherichia coli. Cell Calcium 2002, 32:183-192.
63. Trombe M.C. Characterization of a calcium porter of Streptococcus pneumoniae involved in calcium regulation of growth and competence. J. Gen. Microbiol. 1993, 139:433-439.
64. Tisa L.S. Calcium transport by Frankia sp. strain EAN1pec. Curr. Microbiol. 1998, 37:12-16.
65. Matsushita T., Hirata H., Kusaka I. Calcium channels in bacteria: purification and characterization. Ann. N. Y. Acad. Sci. 1989, 560:426-429.
66. Kanamaru K., Kashiwagi S., Mizuno T. The cyanobacterium, Synechococcus sp. PCC7942, possesses two distinct genes encoding cation-transporting P-type ATPases. FEBS Lett. 1993, 330:99-104.
67. Ambudkar S.V., Lynn A.R., Maloney P.C., Rosen B.P. Reconstitution of ATP-dependent calcium transport from streptococci. Biol. Chem. 1986, 261:15596-15600.
68. Houng H.S., Lynn A.R., Rosen B.P. ATP-driven calcium transport in membrane vesicles of Streptococcus sanguis. J. Bacteriol. 1986, 168:1040-1044.
69. Rosen B.P. Bacterial calcium transport. Biochim. Biophys. Acta 1987, 906:101-110.
70. 2+ channel. Microbiology 2003, 149:1147-1153.
71. Chang Y., Bruni R., Kloss B., Assur Z., Kloppmann E., Rost B., Hendrickson W.A., Liu Q. Structural basis for a pH-sensitive calcium leak across membranes. Science 2014, 344:1131-1135.
72. Palmgren M.G., Axelsen K.B. Evolution of P-type ATPases. Biochim. Biophys. Acta 1998, 1365:37-45.
73. Geisler M., Koenen W., Richter J., Schumann J. Expression and characterization of a Synechocystis PCC 6803 P-type ATPase in E. coli plasma membranes. Biochim. Biophys. Acta 1998, 1368:267-275.
74. (2+)-ATPases. J. Mol. Biol. 1993, 234:1284-1289.
75. 2+-ATPase of Flavobacterium odoratum. J. Biol. Chem. 1996, 271:3945-3951.
76. 2+-ATPase from Flavobacterium odoratum. J. Biol. Chem. 1996, 271:5095-5100.
77. (2+)-binding site. J. Biol. Chem. 2011, 286:1609-1617.
78. Giotis E.S., Muthaiyan A., Blair I.S., Wilkinson B.J., McDowell D.A. Genomic and proteomic analysis of the Alkali-Tolerance Response (AlTR) in Listeria monocytogenes 10403S. BMC Microbiol. 2008, 8:102.
79. (2+)-transport ATPase in Bacillus subtilis during sporulation. Cell Calcium 2002, 32:93.
80. (2+)-transporting ATPase. J. Bacteriol. 1994, 176:4430-4436.
81. Hein K.L., Nissen P., Morth J.P. Purification, crystallization and preliminary crystallographic studies of a PacL homologue from Listeria monocytogenes. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2012, 68:424-427.
82. Driessen A.J.M., Devrij W., Konings W.N. Incorporation of beef-heart cytochrome-C Oxidase as a proton-motive force-generating mechanism in bacterial-membrane vesicles. Proc. Natl. Acad. Sci. U S A 1985, 82:7555-7559.
83. Birge R.R., Govender D.S.K., Izgi K.C., Tan E.H.L. Role of calcium in the proton pump of bacteriorhodopsin. Microwave evidence for a cation-gated mechanism. J. Phys. Chem. 1996, 100:9990-10004.
84. + antiporter from Bacillus subtilis. Eur. J. Biochem. 1986, 156:95-100.
85. + antiporters from cyanobacteria. J. Biol. Chem. 2004, 279:4330-4338.
86. Brey R.N., Rosen B.P. Cation/proton antiport systems in Escherichia coli. Properties of the calcium/proton antiporter. J. Biol. Chem. 1979, 254:1957-1963.
87. van Veen H.W., Abee T., Kortstee G.J., Konings W.N., Zehnder A.J. Translocation of metal phosphate via the phosphate inorganic transport system of Escherichia coli. Biochemistry 1994, 33:1766-1770.
88. + antiporter of the CaCA family. Arch. Microbiol. 2009, 191:649-657.
89. + antiporter-deficient strains by the overexpressed gene. J. Biol. Chem. 1993, 268:11296-11303.
90. Radchenko M.V., Tanaka K., Waditee R., Oshimi S., Matsuzaki Y., Fukuhara M., Kobayashi H., Takabe T., Nakamura T. Potassium/proton antiport system of Escherichia coli. J. Biol. Chem. 2006, 281:19822-19829.
91. Ohyama T., Igarashi K., Kobayashi H. Physiological role of the chaA gene in sodium and calcium circulations at a high pH in Escherichia coli. J. Bacteriol. 1994, 176:4311-4315.
92. Bolhuis H., van Veen H.W., Brands J.R., Putman M., Poolman B., Driessen A.J., Konings W.N. Energetics and mechanism of drug transport mediated by the lactococcal multidrug transporter LmrP. J. Biol. Chem. 1996, 271:24123-24128.
93. Schaedler T.A., Tong Z., van Veen H.W. The multidrug transporter LmrP protein mediates selective calcium efflux. J. Biol. Chem. 2012, 287:27682-27690.
94. Van Veen H.W., Abee T., Kortstee G.J., Konings W.N., Zehnder A.J. Characterization of two phosphate transport systems in Acinetobacter johnsonii 210A. J. Bacteriol. 1993, 175:200-206.
95. Kay W.W., Ghei O.K. Inorganic cation transport and the effects on C4 dicarboxylate transport in Bacillus subtilis. Can. J. Microbiol. 1981, 27:1194-1201.
96. (2+) in E. coli. Biochim. Biophys Acta 2008, 1778:1415-1422.
97. Matsushita T., Hirata H., Kusaka I. Calcium channel blockers inhibit bacterial chemotaxis. FEBS Lett. 1988, 236:437-440.
98. Xi C., Schoeters E., Vanderleyden J., Michiels J. Symbiosis-specific expression of Rhizobium etli casA encoding a secreted calmodulin-related protein. Proc. Natl. Acad. Sci. U S A 2000, 97:11114-11119.
99. Yonekawa T., Ohnishi Y., Horinouchi S. A calmodulin-like protein in the bacterial genus Streptomyces. FEMS Microbiol. Lett. 2005, 244:315-321.
100. 2+-mediated regulation of spore germination and aerial hypha formation in Streptomyces coelicolor. J. Bacteriol. 2008, 190:4061-4068.
101. Kretsinger R.H. Calcium-binding proteins. Annu. Rev. Biochem. 1976, 45:239-266.
102. Kawasaki H., Nakayama S., Kretsinger R.H. Classification and evolution of EF-hand proteins. Biometals 1998, 11:277-295.
103. Rigden D.J., Woodhead D.D., Wong P.W.H., Galperin M.Y. New structural and functional contexts of the Dx[DN]xDG linear motif: insights into evolution of calcium-binding proteins. PloS One 2011, 6.
104. 2+ binding affinity. Plos One 2014, 9.
105. Nakayama S., Kawasaki H., Kretsinger R.H. Evolution of EF-Hand Proteins 2000, Springer Berlin Heidelberg, Berlin.
106. Rigden D.J., Galperin M.Y. The DxDxDG motif for calcium binding: Multiple structural contexts and implications for evolution. J. Mol. Biol. 2004, 343:971-984.
107. 2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 2007, 405:199-221.
108. Chen Y.Y., Xue S.H., Zhou Y.B., Yang J.J. Calciomics: prediction and analysis of EF-hand calcium binding proteins by protein engineering. Sci. China Chem. 2010, 53:52-60.
109. Leadlay P.F., Roberts G., Walker J.E. Isolation of a novel calcium-binding protein from Streptomyces erythreus. FEBS Lett. 1984, 178:157-160.
110. van Asselt E.J., Dijkstra B.W. Binding of calcium in the EF-hand of Escherichia coli lytic transglycosylase Slt35 is important for stability. FEBS Lett. 1999, 458:429-435.
111. Lytle B.L., Volkman B.F., Westler W.M., Heckman M.P., Wu J.H. Solution structure of a type I dockerin domain, a novel prokaryotic, extracellular calcium-binding domain. J. Mol. Biol. 2001, 307:745-753.
112. Momma K., Mikami B., Mishima Y., Hashimoto W., Murata K. Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1 at 2.0A resolution. J. Mol. Biol. 2002, 316:1051-1059.
113. Murzin A.G. Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 1992, 14:191-201.
114. Chaudhuri I., Soding J., Lupas A.N. Evolution of the beta-propeller fold. Proteins 2008, 71:795-803.
115. Kurakata Y., Uechi A., Yoshida H., Kamitori S., Sakano Y., Nishikawa A., Tonozuka T. Structural Insights into the substrate specificity and function of Escherichia coli K12 YgjK, a glucosidase belonging to the glycoside hydrolase family 63. J. Mol. Biol. 2008, 381:116. (383, 745-745).
116. Suzuki R., Katayama T., Kitaoka M., Kumagai H., Wakagi T., Shoun H., Ashida H., Yamamoto K., Fushinobu S. Crystallographic and mutational analyses of substrate recognition of endo-alpha-N-acetylgalactosaminidase from Bifidobacterium longum. J. Biochem. 2009, 146:389-398.
117. Li N., Yun P., Nadkarni M.A., Ghadikolaee N.B., Nguyen K.A., Lee M., Hunter N., Collyer C.A. Structure determination and analysis of a haemolytic gingipain adhesin domain from Porphyromonas gingivalis. Mol. Microbiol. 2010, 76:861-873.
118. 2+-binding loop for folding of Tk-subtilisin from a hyperthermophilic archaeon. Biochemistry 2009, 48:10637-10643.
119. Ochiai A., Itoh T., Maruyama Y., Kawamata A., Mikami B., Hashimoto W., Murata K. A novel structural fold in polysaccharide lyases-Bacillus subtilis family 11 rhamnogalacturonan lyase YesW with an eight-bladed beta-propeller. J. Biol. Chem. 2007, 282:37134-37145.
120. Orans J., Johnson M.D.L., Coggan K.A., Sperlazza J.R., Heiniger R.W., Wolfgang M.C., Redinbo M.R. Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. Proc. Natl. Acad. Sci. U S A 2010, 107:1065.
121. Chenal A., Guijarro J.I., Raynal B., Delepierre M., Ladant D. RTX calcium binding motifs are intrinsically disordered in the absence of calcium: implication for protein secretion. J. Biol. Chem. 2009, 284:1781-1789.
122. Blenner M.A., Shur O., Szilvay G.R., Cropek D.M., Banta S. Calcium-induced folding of a beta roll motif requires C-terminal entropic stabilization. J. Mol. Biol. 2010, 400:244-256.
123. Thomas S., Bakkes P.J., Smits S.H.J., Schmitt L. Equilibrium folding of pro-HlyA from Escherichia coli reveals a stable calcium ion dependent folding intermediate. BBA-Proteins Proteomics 2014, 1844:1500-1510.
124. Brennan M.J., Delogu G. The PE multigene family: a 'molecular mantra' for mycobacteria. Trends Microbiol. 2002, 10:246-249.
125. Bachhawat N., Singh B. Mycobacterial PE_PGRS proteins contain calcium-binding motifs with parallel beta-roll folds. Genomics Proteomics Bioinform. 2007, 5:236-241.
126. Tian C., Jian-Ping X. Roles of PE_PGRS family in Mycobacterium tuberculosis pathogenesis and novel measures against tuberculosis. Microb. Pathog. 2010, 49:311-314.
127. Bottai D., Brosch R. Mycobacterial PE, PPE and ESX clusters: novel insights into the secretion of these most unusual protein families. Mol. Microbiol. 2009, 73:325-328.
128. Meena L.S. An overview to understand the role of PE_PGRS family proteins in Mycobacterium tuberculosis H Rv and their potential as new drug targets. Biotechnol. Appl. Biochem. 2014.
129. Copin R., Coscolla M., Seiffert S.N., Bothamley G., Sutherland J., Mbayo G., Gagneux S., Ernst J.D. Sequence diversity in the pe_pgrs genes of Mycobacterium tuberculosis is independent of human T cell recognition. MBio 2014, 5.
130. Suman S.K., Ravindra D., Sharma Y., Mishra A. Association properties and unfolding of a betagamma-crystallin domain of a Vibrio-specific protein. PloS One 2013, 8:e53610.
131. Mishra A., Suman S.K., Aravind P., Sharma Y. From microbial to lens βγ-crystallins: presence of a universal calcium-binding motif in βγ-crystallin superfamily. Curr. Trends Sci. 2009, 6.
132. Wistow G. Evolution of a protein superfamily: relationships between vertebrate lens crystallins and microorganism dormancy proteins. J. Mol. Biol. 1990, 30:140-145.
133. Wenk M., Baumgartner R., Holak T.A., Huber R., Jaenicke R., Mayr E.M. The domains of protein S from Myxococcus xanthus: structure, stability and interactions. J. Mol. Biol. 1999, 286:1533-1545.
134. Barnwal R.P., Jobby M.K., Devi K.M., Sharma Y., Chary K.V. Solution structure and calcium-binding properties of M-crystallin, a primordial betagamma-crystallin from archaea. J. Mol. Biol. 2009, 386:675-689.
135. Srivastava A.K., Sharma Y., Chary K.V. A natively unfolded betagamma-crystallin domain from Hahella chejuensis. Biochemistry 2010, 49:9746-9755.
136. Lin Y.P., Raman R., Sharma Y., Chang Y.F. Calcium binds to leptospiral immunoglobulin-like protein, LigB, and modulates fibronectin binding. J. Biol. Chem. 2008, 283:25140-25149.
137. Halaby D.M., Mornon J.P. The immunoglobulin superfamily: an insight on its tissular, species, and functional diversity. J. Mol. Biol. 1998, 46:389-400.
138. Halaby D.M., Poupon A., Mornon J. The immunoglobulin fold family: sequence analysis and 3D structure comparisons. Protein Eng. 1999, 12:563-571.
139. Matsunaga J., Barocchi M.A., Croda J., Young T.A., Sanchez Y., Siqueira I., Bolin C.A., Reis M.G., Riley L.W., Haake D.A., Ko A.I. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol. Microbiol. 2003, 49:929-945.
140. Holmgren A., Branden C.I. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 1989, 342:248-251.
141. Hofmann B.E., Bender H., Schulz G.E. Three-dimensional structure of cyclodextrin glycosyltransferase from Bacillus circulans at 3.4 A resolution. J. Mol. Biol. 1989, 209:793-800.
142. Crabbe M.J., Goode D. Protein folds and functional similarity; the Greek key/immunoglobulin fold. Comput. Chem. 1995, 19:343-349.
143. Raman R., Sharma Y., Chang Y.F. Ca-binding and spectral properties of the common region of surface-exposed Lig proteins of leptospira. Commun. Integr. Biol. 2011, 4:331-333.
144. 2+-binding module. Sci. Rep. 2013, 3.
145. Onek L.A., Smith R.J. Calmodulin and calcium mediated regulation in prokaryotes. J. Gen. Microbiol. 1992, 138:1039-1049.
146. Norris V., Grant S., Freestone P., Canvin J., Sheikh F.N., Toth I., Trinei M., Modha K., Norman R.I. Calcium signalling in bacteria. J. Bacteriol. 1996, 178:3677-3682.
147. Norris V., Chen M., Goldberg M., Voskuil J., McGurk G., Holland I.B. Calcium in bacteria: a solution to which problem?. Mol. Microbiol. 1991, 5:775-778.
148. Smith R.J. Calcium and bacteria. Adv. Microb. Physiol. 1995, 37:83-133.
149. Killian J.A., Koorengevel M.C., Bouwstra J.A., Gooris G., Dowhan W., de Kruijff B. Effect of divalent cations on lipid organization of cardiolipin isolated from Escherichia coli strain AH930. Biochim. Biophys. Acta 1994, 1189:225-232.
150. 2+-dependent biofilm development in sea water. Proc. Natl. Acad. Sci. U S A 2003, 100:14357-14362.
151. Lu D., Shang G., Zhang H., Yu Q., Cong X., Yuan J., He F., Zhu C., Zhao Y., Yin K., Chen Y., Hu J., Zhang X., Yuan Z., Xu S., Hu W., Cang H., Gu L. Structural insights into the T6SS effector protein Tse3 and the Tse3-Tsi3 complex from Pseudomonas aeruginosa reveal a calcium-dependent membrane-binding mechanism. Mol. Microbiol. 2014, 92:1092-1112.
152. Josefsson E., O'Connell D., Foster T.J., Durussel I., Cox J.A. The binding of calcium to the B-repeat segment of SdrD, a cell surface protein of Staphylococcus aureus. J. Biol. Chem. 1998, 273:31145-31152.
153. 2+-dependent inhibitory site. J. Biol. Chem. 1998, 273:6821-6829.
154. Ni Eidhin D., Perkins S., Francois P., Vaudaux P., Hook M., Foster T.J. Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol. Microbiol. 1998, 30:245-257.
155. Arrizubieta M.J., Toledo-Arana A., Amorena B., Penades J.R., Lasa I. Calcium inhibits bap-dependent multicellular behavior in Staphylococcus aureus. J. Bacteriol. 2004, 186:7490-7498.
156. Torres A.G., Perna N.T., Burland V., Ruknudin A., Blattner F.R., Kaper J.B. Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol. Microbiol. 2002, 45:951-966.
157. Wolfgang M.C., Lee V.T., Gilmore M.E., Lory S. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev. Cell 2003, 4:253-263.
158. Sherman M.Y., Goldberg A.L. Heat shock of Escherichia coli increases binding of dnaK (the hsp70 homolog) to polypeptides by promoting its phosphorylation. Proc. Natl. Acad. Sci. U S A 1993, 90:8648-8652.
159. Saha A.K., Dowling J.N., Mukhopadhyay N.K., Glew R.H. Demonstration of two protein kinases in extracts of Legionella micdadei. J. Gen. Microbiol. 1988, 134:1275-1281.
160. Flego D., Pirhonen M., Saarilahti H., Palva T.K., Palva E.T. Control of virulence gene expression by plant calcium in the phytopathogen Erwinia carotovora. Mol. Microbiol. 1997, 25:831-838.
161. Ramstad S., Futsaether C.M., Johnsson A. Porphyrin sensitization and intracellular calcium changes in the prokaryote Propionibacterium acnes. J. Photochem. Photobiol. B 1997, 40:141-148.
162. (2+) mobilization and kinase activity during acylated homoserine lactone-dependent quorum sensing in Serratia liquefaciens. J. Biol. Chem. 2001, 276:6468-6472.
163. Watkins N.J., Knight M.R., Trewavas A.J., Campbell A.K. Free calcium transients in chemotactic and non-chemotactic strains of Escherichia coli determined by using recombinant aequorin. Biochem. J. 1995, 306(Pt 3):865-869.
164. 2+ transients and inhibit growth in E. coli. Arch. Biochem. Biophys. 2007, 468:107-113.
165. 2+ regulates protein expression in E. coli through release from inclusion bodies. Biochem. Biophys. Res. Commun. 2007, 360:33-39.
166. Prost L.R., Miller S.I. The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell. Microbiol. 2008, 10:576-582.
167. 2+. J. Biol. Chem. 1997, 272:1440-1443.
168. Theodorou M.C., Panagiotidis C.A., Panagiotidis C.H., Pantazaki A.A., Kyriakidis D.A. Involvement of the AtoS-AtoC signal transduction system in poly-(R)-3-hydroxybutyrate biosynthesis in Escherichia coli. Biochim. Biophys. Acta 2006, 1760:896-906.
169. 2+ channels in the plasma membranes of Escherichia coli. Biophys. J. 1995, 69:754-766.
170. 2+ transients affect poly-(R)-3-hydroxybutyrate regulation by the AtoS-AtoC system in Escherichia coli. Biochem. J. 2009, 417:667-672.
171. 2+-dependent expression of the CIRCE regulon in Streptococcus pneumoniae. Mol. Microbiol. 2005, 55:456-468.
172. Ikura M. Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 1996, 21:14-17.
173. Yonekawa T., Ohnishi Y., Horinouchi S. A calcium-binding protein with four EF-hand motifs in Streptomyces ambofaciens. Biosci. Biotech. Biochem. 2001, 65:156-160.
174. Utsumi R., Brissette R.E., Rampersaud A., Forst S.A., Oosawa K., Inouye M. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 1989, 245:1246-1249.
175. 2(+)-enhanced phosphorylation of a chimeric protein kinase involved with bacterial signal transduction. J. Biol. Chem. 1991, 266:7633-7637.
176. Checchetto V., Formentin E., Carraretto L., Segalla A., Giacometti G.M., Szabo I., Bergantino E. Functional characterization and determination of the physiological role of a calcium-dependent potassium channel from cyanobacteria. Plant Physiol. 2013, 162:953-964.
177. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 2002, 417:515-522.
178. Parfenova L.V., Abarca-Heidemann K., Crane B.M., Rothberg B.S. Molecular architecture and divalent cation activation of TvoK, a prokaryotic potassium channel. J. Biol. Chem. 2007, 282:24302-24309.
179. 2+ indicators for live cell imaging. J. Am. Chem. Soc. 2013, 135:46-49.
180. (2+) binding green fluorescent proteins. Arch. Biochem. Biophys. 2009, 486:27-34.
181. 2+)-ATPase from Flavobacterium odoratum. J. Biol. Chem. 1992, 267:15923-15931.
182. (2+)-ATPase LMCA1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2011, 67:718-722.
183. Henderson R., Baldwin J.M., Ceska T.A., Zemlin F., Beckmann E., Downing K.H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy. J. Mol. Biol. 1990, 213:899-929.
184. Stuart J.A., Vought B.W., Zhang C.F., Birge R.R. The active-site of bacteriorhodopsin-2-photon spectroscopic evidence for a positively charged chromophore binding-site mediated by calcium. Biospectroscopy 1995, 1:9-28.
185. 2+-transport in membrane-vesicles of Streptococcus cremoris fused with bacteriorhodopsin proteoliposomes. Biochim. Biophys. Acta 1985, 808:1-12.
186. 2+ efflux and its pH regulation. Proc. Natl. Acad. Sci. U S A 2013, 110:11367-11372.
187. Swan D.G., Cortes J., Hale R.S., Leadlay P.F. Cloning, characterization, and heterologous expression of the Saccharopolyspora erythraea (Streptomyces erythraeus) gene encoding an EF-hand calcium-binding protein. J. Bacteriol. 1989, 171:5614-5619.
188. Roujeinikova A., Raasch C., Sedelnikova S., Liebl W., Rice D.W. Crystal structure of Thermotoga maritima 4-alpha-glucanotransferase and its acarbose complex: implications for substrate specificity and catalysis. J. Mol. Biol. 2002, 321:149-162.
189. Petosa C., Collier R.J., Klimpel K.R., Leppla S.H., Liddington R.C. Crystal structure of the anthrax toxin protective antigen. Nature 1997, 385:833-838.
190. Vyas N.K., Vyas M.N., Quiocho F.A. A novel calcium binding site in the galactose-binding protein of bacterial transport and chemotaxis. Nature 1987, 327:635-638.
191. Baumann U., Wu S., Flaherty K.M., McKay D.B. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J. 1993, 12:3357-3364.
192. Sadeghi L., Khajeh K., Mollania N., Dabirmanesh B., Ranjbar B. Extra EF hand unit (DX) mediated stabilization and calcium independency of alpha-amylase. Mol. Biotechnol. 2013, 53:270-277.
193. Bagby S., Harvey T.S., Eagle S.G., Inouye S., Ikura M. NMR-derived three-dimensional solution structure of protein S complexed with calcium. Structure 1994, 2:107-122.
194. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 1996, 84:165-174.
195. Gunn J.S., Miller S.I. PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J. Bacteriol. 1996, 178:6857-6864.
196. Scotter A.J., Guo M., Tomczak M.M., Daley M.E., Campbell R.L., Oko R.J., Bateman D.A., Chakrabartty A., Sykes B.D., Davies P.L. Metal ion-dependent, reversible, protein filament formation by designed beta-roll polypeptides. BMC Struct. Biol. 2007, 7:63. 10.1186/1472-6807-7-63.