Identification of the subunit loci in the extracellular multisubunit hemoglobin from annelid Perinereis aibuhitensis

Arch Biochem Biophys. 1996 Nov 1;335(1):23-31. doi: 10.1006/abbi.1996.0478.

Abstract

Giant hemoglobin (Hb) from Perinereis aibuhitensis is made of several types of protein components including single-chain globin (a), disulfide-bridged globin trimer (A-b-B), disulfide-bridged dimers of nonglobin chain (or linkers; L1-L1, L2-L2, and L1-L2), and oligomers of L1-L2 [(L1-L2)n]. The intact form of this giant Hb is a two-tiered hexagonal structure composed of 12 identical units, or so-called submultiples (six submultiples to a tier). To obtain a view of the three-dimensional architectural arrangement of these components in the intact form, we identified the subunit loci by using two mutually complementary chemical modifications and a colloidal gold labeling technique. Using the chemical modifications, we discovered that (i) linkers L1-L2 and L2-L2 were located at the exterior of the Hb, (ii) linker L1-L1 and globin a were buried in the interior, and (iii) linker (L1-L2)n and globin trimer A-b-B were located at both exterior and interior loci. The labeling with an L2-specific colloidal gold revealed the predominant loci of L2 at the outer and inner boundaries between neighboring submultiples in a hexagonal form. By combining these results with those from our previous reports [S. Ebina, K. Matsubara, K. Nagayama, M. Yamaki, and T. Gotoh (1995) Proc. Natl. Acad. Sci. USA 92, 7367-7371; K. Matsubara, M. Yamaki, Nagayama, H. Ishii, K. Imai, T. Gotoh, and S. Ebina (1996), in press], we deduced the following conclusions concerning the Hb architecture. The L1-L1 chains perhaps together with (L1-L2)n chains form a scaffold on which submultiples assemble into a two-tiered hexagonal arrangement, probably by connecting the carbohydrates in globin a. The L1-L2 and L2-L2 chains reinforce the connections of the submultiples by binding carbohydrates, perhaps those carbohydrates in globin A. We proposed to call this type of non-protein-dependent structural level as seen in such a carbohydrate-glued protein aggregate "protein-plus structure."

MeSH terms

  • Animals
  • Annelida*
  • Cross-Linking Reagents
  • Disulfides
  • Electrophoresis, Polyacrylamide Gel
  • Fluorescein-5-isothiocyanate
  • Globins / chemistry
  • Hemoglobins / chemistry*
  • Hemoglobins / isolation & purification
  • Hemoglobins / ultrastructure*
  • Kinetics
  • Macromolecular Substances
  • Microscopy, Electron
  • Models, Structural

Substances

  • Cross-Linking Reagents
  • Disulfides
  • Hemoglobins
  • Macromolecular Substances
  • Globins
  • Fluorescein-5-isothiocyanate