Biliprotein maturation: the chromophore attachment

Abstract

Summary Biliproteins are a widespread group of brilliantly coloured photoreceptors characterized by linear tetrapyrrolic chromophores, bilins, which are covalently bound to the apoproteins via relatively stable thioether bonds. Covalent binding stabilizes the chromoproteins and is mandatory for phycobilisome assembly; and, it is also important in biliprotein applications such as fluorescence labelling. Covalent binding has, on the other hand, also considerably hindered biliprotein research because autocatalytic chromophore additions are rare, and information on enzymatic addition by lyases was limited to a single example, an EF‐type lyase attaching phycocyanobilin to cysteine‐α84 of C‐phycocyanin. The discovery of new activities for the latter lyases, and of new types of lyases, have reinvigorated research activities in the subject. So far, work has mainly concentrated on cyanobacterial phycobiliproteins. Methodological advances in the process, however, as well as the finding of often large numbers of homologues, opens new possibilities for research on the subsequent assembly/disassembly of the phycobilisome in cyanobacteria and red algae, on the assembly and organization of the cryptophyte light‐harvesting system, on applications in basic research such as protein folding, and on the use of phycobiliproteins for labelling.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 110

1. 1.

   Adir N, Vainer R, Lerner N. Refined structure of c-phycocyanin from the cyanobacterium Synechococcus vulcanus at 1.6 A: insights into the role of solvent molecules in thermal stability and co-factor structure. Biochim Biophys Acta. 2002;1556:168-174.

   Not in our library10.1016/s0005-2728(02)00359-6

2. 2.

   Anderson LK, Toole CM. A model for early events in the assembly pathway of cyanobacterial phycobilisomes. Mol Microbiol. 1998;30:467-474.

   Not in our library10.1046/j.1365-2958.1998.01081.x

3. 3.

   Apt KE, Collier JL, Grossman AR. Evolution of phycobiliproteins. J Mol Biol. 1995;248:79-96.

   Not in our library10.1006/jmbi.1995.0203

4. 4.

   Arciero DM, Bryant DA, Glazer AN. In vitro attachment of Bilins to Apophycocyanin. 1. Specific covalent adduct formation at Cysteinyl residues involved in Phycocyanobilin binding in C-Phycocyanin. J Biol Chem. 1988;263:18343-18349.

   Not in our library

5. 5.

   Balabas BE, Montgomery BL, Ong LE, Kehoe DM. CotB is essential for complete activation of green light-induced genes during complementary chromatic adaptation in Fremyella diplosiphon. Mol Microbiol. 2003;50:781-793.

   Not in our library10.1046/j.1365-2958.2003.03718.x

6. 6.

   Beale SI. Biosynthesis of phycobilins. Chem Rev. 1993;93:785-802.

   Not in our library

7. 7.

   Beale SI. Enzymes of chlorophyll biosynthesis. Photosynth Res. 1999;60:43-73.

   Not in our library

8. 8.

   Beale SI, Cornejo J. Biosynthesis of phycobilins. Ferredoxin-mediated reduction of biliverdin catalyzed by extracts of Cyanidium caldarium. J Biol Chem. 1991;266:22328-22332.

   Not in our library

9. 9.

   Bhoo SH, Hirano T, Jeong H, Lee J, Furuya M, Song P. Phytochrome photochromism probed by site-directed mutations and chromophore esterification. J Am Chem Soc. 1997;119:11717-11718.

   Not in our library

10. 10.

    Bienert R, Baier K, Volkmer R, Lockau W, Heinemann U. Crystal structure of NblA from Anabaena sp. PCC 7120, a small protein playing a key role in phycobilisome degradation. J Biol Chem. 2006;281:5216-5223.

    Not in our library10.1074/jbc.m507243200

11. 11.

    Böhm S, Endres S, Scheer H, Zhao K-H. Biliprotein chromophore attachment: chaperone-like function of PecE-subunit of α-phycoerythrocyanin lyaseE. J Biol Chem. 2007;282:25357-25366.

    Not in our library10.1074/jbc.m702669200

12. 12.

    Bryant DA, Cohen-Bazire G, Glazer AN. Characterization of the Biliproteins of Gloeobacter-violaceus chromophore content of a cyanobacterial Phycoerythrin carrying Phycourobilin chromophore. Arch Microbiol. 1981;129:190-198.

    Not in our library

13. 13.

    Chisholm S, Huang K, Martiny A, Kettler G, Coleman M, Keller K, et al. Phycoerythrin linker proteins CpeS and CpeT from Prochlorococcus marinus (strain MIT 9515) (UniProtKB/TrEMBL entries A2BUT8 and A2CBV6). 2006.

    Not in our library

14. 14.

    Cobley JG, Clark AC, Weerasurya S, Queseda FA, Xiao JY, Bandrapali N, et al. CpeR is an activator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon (cpeCDESTR). Mol Microbiol. 2002;44:1517-1531.

    Not in our library10.1046/j.1365-2958.2002.02966.x

15. 15.

    Copeland A, Lucas S, Lapidus A, Barry K, Detter JC, Glavina T, et al. CpeS homolog from Prochlorococcus marinus (strain NATL2A) (UniProtKB/TrEMBL entry Q46H67). 2005.

    Not in our library

16. 16.

    Daltrop O, Allen JW, Willis AC, Ferguson SJ. In vitro formation of a c-type cytochrome. Proc Natl Acad Sci USA. 2002;99:7872-7876.

    Not in our library10.1073/pnas.132259099

17. 17.

    Dammeyer T, Frankenberg-Dinkel N. Insights into phycoerythrobilin biosynthesis point toward metabolic channeling. J Biol Chem. 2006;281:27081-27089.

    Not in our library10.1074/jbc.m605154200

18. 18.

    Dammeyer T, Bagby SC, Sullivan MB, Chisholm SW, Frankenberg-Dinkel N. Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr Biol. 2008.

    Not in our library10.1016/j.cub.2008.02.067

19. 19.

    De Lorimier R, Wilbanks SM, Glazer AN. Genes of the R-Phycocyanin II locus of marine Synechococcus spp. & comparison of protein–chromophore interactions in Phycocyanins differing in Bilin composition. Plant Mol Biol. 1993;21:225-237.

    Not in our library10.1007/bf00019939

20. 20.

    Dolganov N, Grossman AR. A polypeptide with similarity to phycocyanin alpha-subunit phycocyanobilin lyase involved in degradation of phycobilisomes. J Bacteriol. 1999;181:610-617.

    Not in our library10.1128/jb.181.2.610-617.1999

21. 21.

    Douglas SE, Zauner S, Fraunholz M, Beaton M, Penny SL, Deng L-T, et al. The highly reduced genome of an enslaved algal nucleus (UniProtKB/TrEMBL entry Q98RP9). Nature. 2001;410:1091-1096.

    Not in our library10.1038/35074092

22. 22.

    Doust AB, Marai CNJ, Harrop SJ, Wilk KE, Curmi PMB, Scholes GD. Developing a structure–function model for the cryptophyte phycoerythrin 545 using ultrahigh resolution crystallography and ultrafast laser spectroscopy. J Mol Biol. 2004;344:135-153.

    Not in our library10.1016/j.jmb.2004.09.044

23. 23.

    Everroad C, Six C, Partensky F, Thomas JC, Holtzendorff J, Wood AM. Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp. J Bacteriol. 2006;188:3345-3356.

    Not in our library10.1128/jb.188.9.3345-3356.2006

24. 24.

    Fairchild CD, Glazer AN. Nonenzymatic bilin addition to the gamma subunit of an apophycoerythrin. J Biol Chem. 1994a;269:28988-28996.

    Not in our library

25. 25.

    Fairchild CD, Glazer AN. Oligomeric structure, enzyme kinetics, and substrate specificity of the phycocyanin alpha subunit phycocyanobilin lyase. J Biol Chem. 1994b;269:8686-8694.

    Not in our library

26. 26.

    Fairchild CD, Zhao J, Zhou J, Colson SE, Bryant DA, Glazer AN. Phycocyanin α-subunit phycocyanobilin lyase. Proc Natl Acad Sci USA. 1992;89:7017-7021.

    Not in our library10.1073/pnas.89.15.7017

27. 27.

    Falk H. The Chemistry of Linear Oligopyrroles and Bile Pigments. 1989.

    Not in our library

28. 28.

    Ficner R, Huber R. Refined crystal structure of phycoerythrin from Porphyridium cruentum at 2.3 Angström resolution and localization of the gamma subunit. Eur J Biochem. 1993;218:103-106.

    Not in our library10.1111/j.1432-1033.1993.tb18356.x

29. 29.

    Frankenberg N, Lagarias JC, Kadish KM, Smith KM, Guilard R. Biosynthesis and biological functions of bilins. The Porphyrin Handbook. 2003a;211-236.

    Not in our library

30. 30.

    Frankenberg N, Lagarias JC. Phycocyanobilin: ferredoxin oxidoreductase of Anabaena sp. PCC 7120. Biochemical and spectroscopic. J Biol Chem. 2003b;278:9219-9226.

    Not in our library10.1074/jbc.m211643200

31. 31.

    Gindt YM, Zhou J, Bryant DA, Sauer K. Core mutations of Synechococcus sp. PCC 7002 phycobilisomes: a spectroscopic study. J Photochem Photobiol B. 1992;15:75-89.

    Not in our library10.1016/1011-1344(92)87007-v

32. 32.

    Gindt YM, Zhou JH, Bryant DA, Sauer K. Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: assignment of excited state energies to the L(cm), beta(18) and alpha(AP-B) chromophores. Biochim Biophys Acta. 1994;1186:153-162.

    Not in our library10.1016/0005-2728(94)90174-0

33. 33.

    Glazer AN, Stryer L. Fluorescent tandem phycobiliprotein conjugates. Emission wavelength shifting by energy transfer. Biophys J. 1983;43:383-386.

    Not in our library10.1016/s0006-3495(83)84361-6

34. 34.

    Grossman AR, van Waasbergen LG, Kehoe D, Green B, Parson W. Environmental regulation of phycobilisome biosynthesis. Light-Harvesting Antennas in Photosynthesis. 2003;471-493.

    Not in our library

35. 35.

    Hess WR, Partensky F, van der Staay GW, Garcia-Fernandez JM, Borner T, Vaulot D. Coexistence of phycoerythrin and a chlorophyll a/b antenna in a marine prokaryote. Proc Natl Acad Sci USA. 1996;93:11126-11130.

    Not in our library10.1073/pnas.93.20.11126

36. 36.

    Hess WR, Steglich C, Lichtlé C, Partensky F. Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster. Plant Mol Biol. 1999;40:507-521.

    Not in our library10.1023/a:1006252013008

37. 37.

    Hess WR, Rocap G, Ting CS, Larimer F, Stilwagen S, Lamerdin J, Chisholm SW. The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynth Res. 2001;70:53-71.

    Not in our library10.1023/a:1013835924610

38. 38.

    Hu IC, Lee TR, Lin HF, Chiueh CC, Lyu PC. Biosynthesis of fluorescent allophycocyanin alpha-subunits by autocatalytic bilin attachment. Biochemistry. 2006;45:7092-7099.

    Not in our library10.1021/bi052067a

39. 39.

    Inomata K, Noack S, Hammam MA, Khawn H, Kinoshita H, Murata Y, et al. Assembly of synthetic locked chromophores with Agrobacterium phytochromes Agp1 and Agp2. J Biol Chem. 2006;281:28162-28173.

    Not in our library10.1074/jbc.m603983200

40. 40.

    Ishizuka T, Narikawa R, Kohchi T, Katayama M, Ikeuchi M. Cyanobacteriochrome TePixJ of Thermosynechococcus elongatus harbors phycoviolobilin as a chromophore. Plant Cell Physiol. 2007;48:1385-1390.

    Not in our library10.1093/pcp/pcm106

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.