Fluorescent fusion proteins of soluble guanylyl cyclase indicate proximity of the heme nitric oxide domain and catalytic domain

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Haase, Tobias ^a   Haase, Nadine ^a   Kraehling, Jan Robert ^a   Behrends, Soenke ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYAN FLUORESCENT PROTEIN; GUANYLATE CYCLASE; HETERODIMER; HYBRID PROTEIN; MONOMER; NITRIC OXIDE; YELLOW FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACULOVIRUS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CYTOSOLIC FRACTION; ENZYME ACTIVITY; ENZYME REGULATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; SENSITIZATION; ANIMAL; ARMYWORM; CELL LINE; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; METABOLISM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN TERTIARY STRUCTURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CATALYTIC DOMAIN; CELL LINE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; GUANYLATE CYCLASE; NITRIC OXIDE; PROTEIN STRUCTURE, TERTIARY; SPODOPTERA;

EID: 77955402749     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011617     Document Type: Article

References (41)

1. Garbers DL, Chrisman TD, Wiegn P, Katafuchi T, Albanesi JP, et al. (2006) Membrane guanylyl cyclase receptors: an update. Trends Endocrinol Metab 17: 251-258.
2. Schmidt HH, Hofmann F, Stasch JP (2009) Handbook of Experimental Pharmacology 191. cGMP: generators, effectors and therapeutic implications. Preface. Handb Exp Pharmacol. pp v-vi.
3. Schmidt HH, Schmidt PM, Stasch JP (2009) NO- and haem-independent soluble guanylate cyclase activators. Handb Exp Pharmacol. pp 309-339.
4. Evgenov OV, Pacher P, Schmidt PM, Hasko G, Schmidt HH, et al. (2006) NO independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential. Nat Rev Drug Discov 5: 755-768.
5. Winger JA, Derbyshire ER, Lamers MH, Marletta MA, Kuriyan J (2008) The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase. BMC Struct Biol 8: 42.
6. Karow DS, Pan D, Tran R, Pellicena P, Presley A, et al. (2004) Spectroscopic characterization of the soluble guanylate cyclase-like heme domains from Vibrio cholerae and Thermoanaerobacter tengcongensis. Biochemistry 43: 10203- 10211.
7. Boon EM, Davis JH, Tran R, Karow DS, Huang SH, et al. (2006) Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase beta1 H-NOX domain. J Biol Chem 281: 21892-21902.
8. Nioche P, Berka V, Vipond J, Minton N, Tsai AL, et al. (2004) Femtomolar sensitivity of a NO sensor from Clostridium botulinum. Science 306: 1550-1553.
9. Ma X, Sayed N, Beuve A, van den Akker F (2007) NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism. Embo J 26: 578-588.
10. Shiga T, Suzuki N (2005) Amphipathic alpha-helix mediates the heterodimerization of soluble guanylyl cyclase. Zoolog Sci 22: 735-742.
11. Anantharaman V, Balaji S, Aravind L (2006) The signaling helix: a common functional theme in diverse signaling proteins. Biol Direct 1: 25.
12. Iyer LM, Anantharaman V, Aravind L (2003) Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics 4: 5.
13. Ma X, Sayed N, Baskaran P, Beuve A, van den Akker F (2008) PAS-mediated dimerization of soluble guanylyl cyclase revealed by signal transduction histidine kinase domain crystal structure. J Biol Chem 283: 1167-1178.
14. Lembo AJ, Kurtz CB, Macdougall JE, Lavins BJ, Currie MG, et al. (2010) Efficacy of linaclotide for patients with chronic constipation. Gastroenterology 138: 886-895 e881.
15. Winger JA, Marletta MA (2005) Expression and characterization of the catalytic domains of soluble guanylate cyclase: interaction with the heme domain. Biochemistry 44: 4083-4090.
16. Nikolaev VO, Gambaryan S, Lohse MJ (2006) Fluorescent sensors for rapid monitoring of intracellular cGMP. Nat Methods 3: 23-25.
17. Kolossov VL, Spring BQ, Sokolowski A, Conour JE, Clegg RM, et al. (2008) Engineering redox-sensitive linkers for genetically encoded FRET-based biosensors. Exp Biol Med (Maywood) 233: 238-248.
18. Ma X, Beuve A, van den Akker F (2010) Crystal structure of the signaling helix coiled-coil domain of the beta1 subunit of the soluble guanylyl cyclase. BMC Struct Biol 10: 2.
19. Truong K, Ikura M (2001) The use of FRET imaging microscopy to detect protein-protein interactions and protein conformational changes in vivo. Curr Opin Struct Biol 11: 573-578.
20. Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, et al. (1996) Crystal structure of the Aequorea victoria green fluorescent protein. Science 273: 1392-1395.
21. Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67: 509-544.
22. Wedel B, Humbert P, Harteneck C, Foerster J, Malkewitz J, et al. (1994) Mutation of His-105 in the beta 1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase. Proc Natl Acad Sci U S A 91: 2592-2596.
23. Zhao Y, Schelvis JP, Babcock GT, Marletta MA (1998) Identification of histidine 105 in the beta1 subunit of soluble guanylate cyclase as the heme proximal ligand. Biochemistry 37: 4502-4509.
24. Zhao Y, Marletta MA (1997) Localization of the heme binding region in soluble guanylate cyclase. Biochemistry 36: 15959-15964.
25. Koglin M, Behrends S (2003) A functional domain of the alpha1 subunit of soluble guanylyl cyclase is necessary for activation of the enzyme by nitric oxide and YC-1 but is not involved in heme binding. J Biol Chem 278: 12590-12597.
26. Koglin M, Stasch JP, Behrends S (2002) BAY 41-2272 activates two isoforms of nitric oxide-sensitive guanylyl cyclase. Biochem Biophys Res Commun 292: 1057-1062.
27. Rothkegel C, Schmidt PM, Atkins DJ, Hoffmann LS, Schmidt HH, et al. (2007) Dimerization region of soluble guanylate cyclase characterized by bimolecular fluorescence complementation in vivo. Mol Pharmacol 72: 1181-1190.
28. Kerppola TK (2006) Complementary methods for studies of protein interactions in living cells. Nat Methods 3: 969-971.
29. Haase N, Haase T, Kraehling JR, Behrends S Direct fusion of subunits of heterodimeric nitric oxide sensitive guanylyl cyclase leads to functional enzymes with preserved biochemical and pharmacological properties manuscript in preparation.
30. Zabel U, Hausler C, Weeger M, Schmidt HH (1999) Homodimerization of soluble guanylyl cyclase subunits. Dimerization analysis using a glutathione stransferase affinity tag. J Biol Chem 274: 18149-18152.
31. Lee YC, Martin E, Murad F (2000) Human recombinant soluble guanylyl cyclase: expression, purification, and regulation. Proc Natl Acad Sci U S A 97: 10763-10768.
32. Fernhoff NB, Derbyshire ER, Marletta MA (2009) A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc Natl Acad Sci U S A 106: 21602-21607.
33. Schultz G, Böhme E (1984) In: Methods of Enzymatic Analysis. pp 379-389.
34. Bamberger AM, Koglin M, Kempfert J, Loning T, Scholz H, et al. (2001) Expression and tissue localization of soluble guanylyl cyclase in the human placenta using novel antibodies directed against the alpha(2) subunit. J Clin Endocrinol Metab 86: 909-912.
35. Youvan DC, Silva CM, Bylina EJ, Coleman WJ, Dilworth MR, Yang MM (1997) Calibration of fluorescence resonance energy transfer in microscopy using genetically engineered GFP derivatives on nickel chelating beads. Biotechnology et alia 3: 1-18.
36. Efendiev R, Cinelli AR, Leibiger IB, Bertorello AM, Pedemonte CH (2006) FRET analysis reveals a critical conformational change within the Na,K-ATPase alpha1 subunit N-terminus during GPCR-dependent endocytosis. FEBS Lett 580: 5067-5070.
37. Sorkina T, Doolen S, Galperin E, Zahniser NR, Sorkin A (2003) Oligomerization of dopamine transporters visualized in living cells by fluorescence resonance energy transfer microscopy. J Biol Chem 278: 28274-28283.
38. Elangovan M, Wallrabe H, Chen Y, Day RN, Barroso M, et al. (2003) Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy. Methods 29: 58-73.
39. Periasamy A, Wallrabe H, Chen Y, Barroso M (2008) Chapter 22: Quantitation of protein-protein interactions: confocal FRET microscopy. Methods Cell Biol 89: 569-598.
40. Patterson GH, Piston DW, Barisas BG (2000) Forster distances between green fluorescent protein pairs. Anal Biochem 284: 438-440.
41. Förster T (1948) Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Physik 6(2): 55-75.