Novel dissociation mechanism of a polychaetous annelid extracellular haemoglobin

FEBS Journal

Volumn 273, Issue 7, 2006, Pages 1582-1596

  Rousselot, Morgane ^a,b   Le Guen, Dominique ^a   Chabasse, Christine ^a   Zal, Franck ^a  

^a STATION BIOLOGIQUE DE ROSCOFF   (France)

^b NONE   (France)

Author keywords

Dissociation; ESI MS; Hemoglobin; MALLS; Polychaete

Indexed keywords

GLOBIN; HEMOGLOBIN; PROTEIN SUBUNIT; UREA; DIVALENT CATION;

ALKALINITY; ANNELID WORM; ARTICLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; GEL FILTRATION; LASER; LIGHT SCATTERING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYCHAETA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROPHOTOMETRY; ANIMAL; CHEMISTRY; GEL CHROMATOGRAPHY; METABOLISM; MOLECULAR WEIGHT; PH; ULTRASTRUCTURE;

ANNELIDA; ARENICOLA; ARENICOLA MARINA; LUMBRICUS; POLYCHAETA;

ANIMALS; CATIONS, DIVALENT; CHROMATOGRAPHY, GEL; HEMOGLOBINS; HYDROGEN-ION CONCENTRATION; MOLECULAR WEIGHT; POLYCHAETA; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 33646895027     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05151.x     Document Type: Article

References (52)

1. Vinogradov SN, Sharma PK & Walz DA (1991) Iron and heme contents of the extracellular hemoglobins and chlorocruorins of annelids. Comp Biochem Physiol B 98, 187-194.
2. Lamy JN, Green BN, Toulmond A, Wall JS, Weber RE & Vinogradov SN (1996) Giant hexagonal bilayer hemoglobins. Chem Rev 96, 3113-3124.
3. Royer WE Jr, Strand K, van Heel M & Hendrickson WA (2000) Structural hierarchy in erythrocruorin, the giant respiratory assemblage of annelids. Proc Natl Acad Sci USA 97, 7107-7111.
4. Zal F, Green BN, Lallier FH, Vinogradov SN & Toulmond A (1997) Quaternary structure of the extracellular haemoglobin of the lugworm Arenicola marina: a multi-angle-laser-light-scattering and electrospray-ionisation-mass- spectrometry analysis. Eur J Biochem 243, 85-92.
5. Kuchumov AR, Taveau JC, Lamy JN, Wall JS, Weber RE & Vinogradov SN (1999) The role of linkers in the reassembly of the 3.6 MDa hexagonal bilayer hemoglobin from Lumbricus terrestris. J Mol Biol 289, 1361-1374.
6. Zhu H, Ownby DW, Riggs CK, Nolasco NJ, Stoops JK & Riggs AF (1996) Assembly of the gigantic hemoglobin of the earthworm Lumbricus terrestris. Roles of subunit equilibria, non-globin linker chains, and valence of the heme iron. J Biol Chem 271, 30007-30021.
7. Green BN, Bordoli RS, Hanin LG, Lallier FH, Toulmond A & Vinogradov SN (1999) Electrospray ionization mass spectrometric determination of the molecular mass of the approximately 200-kDa globin dodecamer subassemblies in hexagonal bilayer hemoglobins. J Biol Chem 274, 28206-28212.
8. Kihm AJ, Kong Y, Hong W, Russell JE, Rouda S, Adachi K, Simon MC, Blobel GA & Weiss MJ (2002) An abundant erythroid protein that stabilizes free alpha-haemoglobin. Nature 417, 758-763.
9. Weber RE & Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81, 569-628.
10. Vinogradov SN, Shlom JM & Doyle M (1979) Dissociation of the extracellular hemoglobin of Arenicola marina. Comp Biochem Physiol 65B, 145-150.
11. Roche J, Wurmser S, Fine JM & Autran R (1963) [Recent Research on the Electron Microscopic Study of the Hemoglobin (Erythrocruorine) of Arenicola Marina L. & Its Dissociation.]. C R Seances Soc Biol Fil 157, 1419-1421.
12. Zal F, Lallier FH & Toulmond A (2000) French patent no. 00/07031. Utilisation Comme Substitut Sanguin d'une Hémoglobine Extracellulaire de Poids Moléculaire Élevé. International Patent, PCT/FR01/01505.
13. Kapp OH, Polidori G, Mainwaring MG, Crewe AV & Vinogradov SN (1984) The reassociation of Lumbricus terrestris hemoglobin dissociated at alkaline pH. J Biol Chem 259, 628-639.
14. Sharma PK, Kuchumov AR, Chottard G, Martin PD, Wall JS & Vinogradov SN (1996) The role of the dodecamer subunit in the dissociation and reassembly of the hexagonal bilayer structure of Lumbricus terrestris hemoglobin. J Biol Chem 271, 8754-8762.
15. Vinogradov SN, Sharma PK, Qabar AN, Wall JS, Westrick JA, Simmons JH & Gill SJ (1991) A dodecamer of globin chains is the principal functional subunit of the extracellular hemoglobin of Lumbricus terrestris. J Biol Chem 266, 13091-13096.
16. Strand K, Knapp JE, Bhyravbhatla B & Royer WE Jr (2004) Crystal structure of the hemoglobin dodecamer from Lumbricus erythrocruorin: allosteric core of giant annelid respiratory complexes. J Mol Biol 344, 119-134.
17. Zhao XJ, Raitt DPVB, Clewell AS, Kwast KE & Poyton RO (1996) Function and expression of flavohemoglobin in Saccharomyces cerevisiae. Evidence for a role in the oxidative stress response. J Biol Chem 271, 25131-25138.
18. Slitine FE & Toulmond A (1991) Two-dimensional electrophoresis of Arenicola marina extracellular hemoglobin: separation of chains with identical molecular mass but different isoelectric point. Comp Biochem Physiol B 100, 631-634.
19. Zal F, Gotoh T & Toulmond A (1999) The novel function of giant hemoglobins from tubeworms and annelids. In Fifth International Congress of Comparative Physiology and Biochemistry, Vol. 124A (Walsh P, ed.), p. 516. Comparative Biochemistry and Physiology, Calgary, Alberta, Canada.
20. Zal F, Leize E, Lallier FH, Toulmond A, Van Dorsselaer A & Childress JJ (1998) S-Sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. Proc Natl Acad Sci USA 95, 8997-9002.
21. Flores JF, Fisher CR, Carney SL, Green BN, Freytag JK, Schaeffer SW & Royer WE Jr (2005) Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc Natl Acad Sci USA 102, 2713-2718.
22. Numoto N, Nakagawa T, Kita A, Sasayama Y, Fukumori Y & Miki K (2005) Crystallization and preliminary X-ray crystallographic analysis of extracellular giant hemoglobin from pogonophoran Oligobrachia mashikoi. Biochim Biophys Acta 1750, 173-176.
23. Daniel E, Lustig A, David MM & Tsfadia Y (2003) Towards a resolution of the long-standing controversy regarding the molecular mass of extracellular erythrocruorin of the earthworm Lumbricus terrestris. Biochim Biophys Acta 1649, 1-15.
24. Polidori G, Mainwaring M, Kosinski T, Schwarz C, Fingal R & Vinogradov SN (1984) The dissociation of the extracellular hemoglobin of Tubifex tubifex at extremes of pH and its reassociation upon return to neutrality. Arch Biochem Biophys 233, 800-814.
25. Ascoli F, Rossi Fanelli MR, Chiancone E, Vecchini P & Antonini E (1978) Studies on erythrocruorin. VI. Ferric derivatives of earthworm erythrocruorin. J Mol Biol 119, 191-202.
26. Zerovnik E & Lapanje S (1986) Interactions of myoglobin with urea and some alkylureas. I. Solvation in urea and alkylurea solutions. Biophys Chem 24, 53-59.
27. Crumpton MJ & Polson A (1965) A comparison of the conformation of sperm whale metmyoglobin with that of apomyoglobin. J Mol Biol 11, 722-729.
28. Kawahara K, Kirshner AG & Tanford C (1965) Dissociation of human CO-hemoglobin by urea, guanidine hydrochloride, and other reagents. Biochemistry 4, 1203-1213.
29. Jeney V, Balla J, Yachie A, Varga Z, Vercellotti GM, Eaton JW & Balla G (2002) Pro-oxidant and cytotoxic effects of circulating heme. Blood 100, 879-887.
30. Suzuki T & Riggs AF (1993) Linker chain L1 of earthworm hemoglobin. Structure of gene and protein: homology with low density lipoprotein receptor. J Biol Chem 268, 13548-13555.
31. Reference withdrawn.
32. Miller YI, Felikman Y & Shaklai N (1995) The involvement of low-density lipoprotein in hemin transport potentiates peroxidative damage. Biochim Biophys Acta 1272, 119-127.
33. Miller YI & Shaklai N (1994) Oxidative crosslinking of LDL protein induced by hemin: involvement of tyrosines. Biochem Mol Biol Int 34, 1121-1129.
34. Paganga G, Rice-Evans C, Rule R & Leake D (1992) The interaction between ruptured erythrocytes and low-density lipoproteins. FEBS Lett 303, 154-158.
35. Green BN, Kuchumov AR, Walz DA, Moens L & Vinogradov SN (1998) A hierarchy of disulfide-bonded subunits: the quaternary structure of Eudistylia chlorocruorin. Biochemistry 37, 6598-6605.
36. Polidori G, Mainwaring MG & Vinogradov SN (1988) The effect of alkaline earth cations and of ionic strength on the dissociation of earthworm hemoglobin at alkaline pH. Comp Biochem Physiol A 89, 541-545.
37. Ochiai T, Hoshina S & Usuki I (1993) Zinc as modulator of oxygenation function and stabilizer of quaternary structure in earthworm hemoglobin. Biochim Biophys Acta 1203, 310-314.
38. Chiancone E, Brenowitz M, Ascoli F, Bonaventura C & Bonaventura J (1980) Amphitrite ornata erythrocruorin. I. Structural properties and characterization of subunit interactions. Biochim Biophys Acta 623, 146-162.
39. Vinogradov SN, Standley PR, Mainwaring MG, Kapp OH & Crewe AV (1985) The molecular size of Myxicola infundibulum chlorocruorin and its subunits. Biochim Biophys Acta 828, 43-50.
40. Guo Y, Yu X, Rihani K, Wang QY & Rong L (2004) The role of a conserved acidic residue in calcium-dependent protein folding for a low density lipoprotein (LDL)-A module: implications in structure and function for the LDL receptor superfamily. J Biol Chem 279, 16629-16637.
41. Chiancone E, Vecchini P, Rossi Fanelli MR & Antonini E (1972) Studies on erythrocruorin. II. Dissociation of earthworm erythrocruorin. J Mol Biol 70, 73-84.
42. Frossard P (1982) The erythrocruorin of Eisenia fetida. II. Properties of the principal subunit. Biochim Biophys Acta 704, 535-541.
43. Bonafe CF, Villas-Boas M, Suarez MC & Silva JL (1991) Reassembly of a large multisubunit protein promoted by nonprotein factors. Effects of calcium and glycerol on the association of extracellular hemoglobin. J Biol Chem 266, 13210-13216.
44. Mainwaring MG, Lugo SD, Fingal RA, Kapp OH & Vinogradov SN (1986) The dissociation of the extracellular hemoglobin of Lumbricus terrestris at acid pH and its reassociation at neutral pH. A new model of its quaternary structure. J Biol Chem 261, 10899-10908.
45. Ochiai T & Weber RE (2002) Effects of magnesium and calcium on the oxygenation reaction of erythrocruorin from the marine polychaete Arenicola marina and the terrestrial oligochaete Lumbricus terrestris. Zool Sci 19, 995-1000.
46. Jouan L, Taveau JC, Marco S, Lallier FH & Lamy JN (2001) Occurrence of two architectural types of hexagonal bilayer hemoglobin in annelids: comparison of 3D reconstruction volumes of Arenicola marina and Lumbricus terrestris hemoglobins. J Mol Biol 305, 757-771.
47. Martin PD, Kuchumov AR, Green BN, Oliver RW, Braswell EH, Wall JS & Vinogradov SN (1996) Mass spectrometric composition and molecular mass of Lumbricus terrestris hemoglobin: a refined model of its quaternary structure. J Mol Biol 255, 154-169.
48. Ebina S, Matsubara K, Nagayama K, Yamaki M & Gotoh T (1995) Carbohydrate gluing, an architectural mechanism in the supramolecular structure of an annelid giant hemoglobin. Proc Natl Acad Sci USA 92, 7367-7371.
49. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
50. Ferrige AG, Seddon MJ, Green BN, Jarvis SA & Skilling J (1992) Disentangling electrospray spectra with maximum entropy. Rapid Commun Mass Spectrom 6, 707-711.
51. Zimm BH (1948) The scattering of light and the radial distribution function of high polymer solutions. J Chem Phys 16, 1093-1099.
52. Valentine RC, Shapiro BM & Stadtman ER (1968) Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7, 2143-2152.