Molecular cloning and characterization of genes encoding FK506-binding proteins (FKBPs) in wheat (Triticum aestivum L.)

Ahn JC, Kim DW, You YN, Seok MS, Park JM, Hwang H, Kim BK, Luan S, Park HS, Cho HS (2010) Classification of rice (Oryza sativa L. Japonica nipponbare) immunophilins (FKBPs, CYPs) and expression patterns under water stress. BMC Plant Biol 10:253

Aviezer K, Kurek I, Erel N, Blecher O, Devos K, Breiman A (1998) Studies on the expression of the wheat prolyl isomerase FKBP73 during plant development. Plant Sci 139:149–158

Blecher O, Erel N, Callebaut I, Aviezer K, Breiman A (1996) A novel plant peptidyl-prolyl-cis–trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Mol Biol 32:493–504

Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

Breiman A, Fawcett TW, Ghirardi ML, Mattoo AK (1992) Plant organelles contain distinct peptidylprolyl cis, trans-isomerases. J Biol Chem 267:21293–21296

Canchi DR, Paschek D, García AE (2010) Equilibrium study of protein denaturation by urea. J Am Chem Soc 132:2338–2344

Chou IT, Gasser CS (1997) Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins. Plant Mol Biol 35:873–892

DeCenzo MT, Park ST, Jarrett BP, Aldape RA, Futer O, Murcko MA, Livingston DJ (1996) FK506-binding protein mutational analysis: defining the active-site residue contributions to catalysis and the stability of ligand complexes. Protein Eng 9:173–180

Dutta T, Kaur H, Singh S, Mishra A, Tripathi JK, Singh N, Pareek A, Singh P (2011) Developmental changes in storage proteins and peptidyl prolyl cis-trans isomerase activity in grains of different wheat cultivars. Food Chem 128:450–457

Edvardsson A, Shapiguzov A, Petersson UA, Schroder WP, Vener AV (2007) Immunophilin AtFKBP13 sustains all peptidyl-prolyl isomerase activity in the thylakoid lumen from Arabidopsis thaliana deficient in AtCyp20-2. Biochem 46:9432–9442

Fanghanel J, Fischer G (2004) Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci 9:3453–3478

Fischer G, Bang H, Mech C (1984) Determination of enzymatic catalysis for the cis–trans isomerization of peptide binding in proline-containing peptides. Biomed Biochim Acta 43:1101–1111

Galat A (2000) Sequence diversification of the FK506-binding proteins in several different genomes. Eur J Biochem 267:4945–4959

Gasser CS, Gunning DA, Budelier KA, Brown SM (1990) Structure and expression of cytosolic cyclophilin/peptidyl-prolyl cis–trans isomerase of higher plants and production of active tomato cyclophilin in Escherichia coli. Proc Natl Acad Sci USA 87:9519–9523

Geisler M, Bailly A (2007) Tete-a-tete: the function of FKBPs in plant development. Trends Plant Sci 12:465–473

Geisler M, Bailly A, Ivanchenko M (2016) Master and servant: regulation of auxin transporters by FKBPs and cyclophilins. Plant Sci 245:1–10

Gollan PJ, Ziemann M, Bhave M (2011) PPIase activities and interaction partners of FK506-binding proteins in the wheat thylakoid. Physiol Plant 143:385–395

Gopalan G, He Z, Battaile KP, Luan S, Swaminathan K (2006) Structural comparison of oxidized and reduced FKBP13 from Arabidopsis thaliana. Proteins Struct Funct Bioinf 65:789–795

Grimwade B, Tatham AS, Freedman RB, Shewry PR, Napier JA (1996) Comparison of the expression patterns of wheat gluten proteins and proteins involved in the secretory pathway in developing caryopses of wheat. Plant Mol Biol 30:1067–1073

Gupta R, Mould RM, He Z, Luan S (2002) A chloroplast FKBP interacts with and affects the accumulation of Rieske subunit of cytochrome bf complex. Proc Nat Acad Sci 99:15806–15811

Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW (1984) Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226:544–547

Harding MW, Galat A, Uehling DE, Schreiber SL (1989) A receptor for the immunosuppressant FK506 is a cis–trans peptidyl-prolyl isomerase. Nature 341:758–760

Harrar Y, Bellini C, Faure J-D (2001) FKBPs: at the crossroads of folding and transduction. Trends Plant Sci 6:426–431

Harrison RK, Stein RL (1990) Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry 29:3813–3816

He Z, Li L, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1248–1267

Hueros G, Rahfeld J, Salamini F, Thompson R (1998) A maize FK506-sensitive immunophilin, mzFKBP-66, is a peptidyl proline cis–trans-isomerase that interacts with calmodulin and a 36-kDa cytoplasmic protein. Planta 205:121–131

Kamphausen T, Fanghänel J, Neumann D, Schulz B, Rahfeld JU (2002) Characterisation of Arabidopsis thaliana AtFKBP42 that is membrane bound and interacts with Hsp90. Plant J 32:63–276

Knutsen JHJ, Rødland GE, Bøe CA, Håland TW, Sunnerhagen P, Grallert B, Boye E (2015) Stress-induced inhibition of translation independently of eIF2α phosphorylation. J Cell Sci 128:4420–4427

Kofron JL, Kuzmic P, Kishore V, Colon-Bonilla E, Rich DH (1991) Determination of kinetic constants for peptidyl prolyl cis–trans isomerases by an improved spectrophotometric method. Biochemistry 30:6127–6134

Kurek I, Aviezer K, Erel N, Herman E, Breiman A (1999) The wheat peptidyl prolyl cis-trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol 119:693–704

Kurek I, Harvey AJ, Lonsdale DM, Breiman A (2000) Isolation and characterization of the wheat prolyl isomerase FK506 binding protein (FKBP) 73 promoter. Plant Mol Biol 42:489–497

Kurek I, Pirkl F, Fischer E, Buchner J, Breiman A (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidyl prolyl cis–trans isomerase activity. Planta 215:119–126

Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144

Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Nat Acad Sci USA 103:12631–12636

Luan S, Kudla J, Gruissem W, Schreiber SL (1996) Molecular characterization of a FKBP-type immunophilin from higher plants. Proc Natl Acad Sci USA 93:6964–6969

Magiri EN, Farchi-Pisanty O, Avni A, Breiman A (2006) The expression of the large rice FK506 binding proteins (FKBPs) demonstrate tissue specificity and heat stress responsiveness. Plant Sci 170:695–704

Mahfouz MM, Kim S, Delauney AJ, Verma DPS (2006) Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18:477–490

Meiri D, Tazat K, Cohen-Peer R, Farchi-Pisanty O, Aviezer-Hagai K, Avni A, Breiman A (2010) Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Mol Biol 72:191–203

Nigam N, Singh A, Sahi C, Chandramouli A, Grover A (2008) SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response. Mol Genet Genom 279:371–383

Rahfeld J-U, Rucknagel KP, Schelbert B, Ludwig B, Hacker J, Mann K, Fischer J (1994) Confirmation of the existence of a third family among peptidyl-prolyl cis/trans isomerases. Amino acid sequence and recombinant production of parvulin. FEBS Lett 352:180–184

Romano P, Gray J, Horton P, Luan S (2005) Plant immunophilins: functional versatility beyond protein maturation. New Phytol 166:753–769

Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529

Rulten SL, Kinloch RA, Tateossian H, Robinson C (2006) The human FK506-binding proteins: characterization of human FKBP19. Mamm Genome 17:322–331

Schreiber SL, Crabtree GR (1992) The mechanism of action of cyclosporin A and FK506. Immunol Today 13:136–142

Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

Seok MS, You YN, Park HJ, Lee SS, Aigen F, Luan S, Ahn JC, Cho HS (2014) AtFKBP16-1, a chloroplast lumenal immunophilin, mediates response to photosynthetic stress by regulating PsaL stability. Physiol Plant 4:620–631

Shapiguzov A, Edvardsson A, Vener AV (2006) Profound redox sensitivity of peptidyl-prolyl isomerase activity in Arabidopsis thylakoid lumen. FEBS Lett 580:3671–3676

Siekierka JJ, Hung SH, Poe M, Lin CS, Sigal NH (1989) A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature 341:755–757

Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39:D561–D568

Unger T, Dym O, Albeck S, Jacobovitch Y, Bernehim R, Marom D, Pisanty O, Breiman A (2010) Crystal structure of the three FK506 binding protein domains of wheat FKBP73: evidence for a unique wFK73_2 domain. J Struct Funct Genomics 11:113–123

Vasudevan D, Fu A, Luan S, Swaminathan K (2012) Crystal structure of Arabidopsis cyclophilin 38 reveals a previously uncharacterized immunophilin fold and a possible autoinhibitory mechanism. Plant Cell 24:2666–2674

Vittorioso P, Cowling R, Faure J-D, Caboche M, Bellini C (1998) Mutation in the Arabidopsis PASTICCINO1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol Cell Biol 18:3034–3043

Wu H, Wensley E, Bhave M (2009) Identification and analysis of genes encoding a novel ER-localised Cyclophilin B in wheat potentially involved in storage protein folding. Plant Sci 176:420–432