Skip to main content
Log in

A Mini Review of the High Mobility Group Proteins of Insects

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

High mobility group (HMG) proteins are an abundant class of chromosomal proteins facilitate assembly of higher order structures. The mammalian HMG proteins have been grouped into three distinct families on the basis of their characteristic functional sequence: the HMGB, the HMGN, and the HMGA family. The HMG proteins of Drosophila melanogaster and Chironomus tentans are the best characterized dipteran insect HMG proteins. Three abundant members of this group of nonhistone proteins were detected in those insects. Two of them belong to the HMGB family and one to the HMGA family. The possible relatedness of these proteins to the formation of higher order nucleoprotein structures and their possible role in the regulation of transcription is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aravind, L., & Landsman, D. (1998). AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res. 26:4413.

    PubMed  Google Scholar 

  • Ashley, T. C., Pendelton, C. G., Jennings, W. W., Saxena, A., & Glover, C. V. C. (1989). Isolation and sequencing of cDNA clones encoding Drosophila chromosomal protein D1. A repeating motif in proteins which recognize AT-DNA. J. Biol. Chem. 264:8394.

    PubMed  Google Scholar 

  • Banks, G. C., Li, Y., & Reeves, R. (2000). Differential in vivo modifications of the HMGI(Y) nonhistone chromatin proteins modulate nucleosome and DNA interactions. Biochemistry 39:8333.

    PubMed  Google Scholar 

  • Bassuk, J., & Mayfield, J. E. (1982). Major high mobility group proteins of Drososphila melanogaster embryonic nuclei. Biochemistry 21:1024.

    PubMed  Google Scholar 

  • Bianchi, M. (1995). The HMG-box domain. In Lilley, D. M. (ed.), DNA-Protein:Structural Interactions: Frontiers in Molecular Biology, IRL Press, Oxford, UK, pp. 177–200.

    Google Scholar 

  • Bruhn, S. L., Pil, P. M., Essigmann, J. M., Housman, D. E., Lippard, S. J. L. (1992). Isolation and characterization of human cDNA clones encoding a high mobility group box protein that recognizes structural distortions to DNA caused by binding of the anticancer agent cisplastin. Proc. Natl. Acad. Sci. U.S.A. 89:2307.

    PubMed  Google Scholar 

  • Bustin, M. (1999). Regulation of DNA-dependent activities by the functional motifs of the high mobility group chromosomal proteins. Mol. Cell Biol. 19:5237.

    PubMed  Google Scholar 

  • Bustin, M., Lehn, D. A., Landsman, D. (1990). Structural features of the HMG chromosomal proteins and their genes. Biochim. Biophys. Acta 1049:231.

    PubMed  Google Scholar 

  • Bustin, M., & Reeves, R. (1996). High mobility group chromosomal proteins: Architectural components that facilitate chromatin function. Prog. Nucleic Acid. Res. 54:35.

    Google Scholar 

  • Cerdan, R., Payet, D., Yang, J. C., Travers, A. A., & Neuhaus, D. (2001). HMG-D complexed to bulge DNA: An NMR model. Protein Sci. 10:504.

    PubMed  Google Scholar 

  • Churchill, M. E. A., Johns, D. M. N., Glaser, T., Hefber, H., Searles, M. A., & Travers, A. A. (1995). HMGD is an architecture specific protein that preferentially binds to DNA containing the dinucleotide TG. EMBO J. 14:1264.

    PubMed  Google Scholar 

  • Claus, P., Schulze, E., & Wisniewski, J. R. (1994). Insect proteins homologous to mammalian high mobility group proteins I/Y (HMGI/Y). Characterization and binding to linear and four-way junction DNA. J. Biol. Chem. 269:33042.

    PubMed  Google Scholar 

  • Ding, H. F., Bustin, M., & Hansen, U. (1997). Alleviation of histone H1–mediated transcriptional repression and chromatin compaction by the acidic activation region of chromosomal protein HMG-14. Mol. Cell Biol. 17:5843.

    PubMed  Google Scholar 

  • Einck, L., & Bustin, M. (1985). The intracellular distribution and function of the high mobility group chromosomal proteins. Exp. Cell Res. 156:295.

    PubMed  Google Scholar 

  • Elton, T. S., & Reeves, R. (1986). Purification and postsynthetic modifications of Friend erythroleukimic cell high mobility group protein HMG-I. Anal. Biochem. 157:53.

    PubMed  Google Scholar 

  • Falciola, L., Murchie, A. I., Lilley, D. M., & Bianchi, M. (1994). Mutational analysis of the DNA-binding domain A of chromosomal protein HMG1. Nucleic Acids Res. 22:285.

    PubMed  Google Scholar 

  • Falvo, J. V., Thanos, D., & Maniatis, T. (1995). Reversal of intrinsic DNA bends in the IFN beta gene enhanser by transcription factors and architectural protein HMGI(Y). Cell 83:1101.

    Article  PubMed  Google Scholar 

  • Ferrari, S., Harley, V. R., Pontiggia, A., Goodfellow, P. N., Lovell-Badge, R., & Bianchi, M. E. (1992). SRY, like HMG1, recognizes sharp angles in DNA. EMBO J. 11:4496.

    Google Scholar 

  • Frank, O., Schwanbeck, R., & Wisniewski, J. R. (1998). Protein footprinting reveals specific binding modes of a high mobility group protein I to DNAs of different conformation. J. Biol. Chem. 273:20015.

    PubMed  Google Scholar 

  • Ghidelli, S., Claus, P., Thies, G., & Wisniewski, J. R. (1997). High mobility group proteins cHMG1a and cHMG1b, and cHMGI, are highly distributed in chromosomes and differentially expressed during ecdysone dependent cell differentiation. Chromosoma 105:369.

    PubMed  Google Scholar 

  • Giese, K., Pagel, J., & Grosschedl, R. (1994). Distinct DNA-binding properties of the high mobility group domain of murine and human SRY sex-determining factors. Proc. Natl. Acad. Sci. U.S.A. 91:3368.

    PubMed  Google Scholar 

  • Glover, C. V. C., Shelton, E. R., & Brutlag, D. L. (1983). Purification and characterization of a type II casein kinase from Drosophila melanogaster. Biochem. Genet. 24:79.

    Google Scholar 

  • Goodwin, G. H., Sanders, C., & Johns, E. W. (1973). A new group of chromatin-associated proteins with a high content of acidic and basic amino acids. Eur. J. Biochem. 38:14.

    PubMed  Google Scholar 

  • Goodwin, G. H., Nicolas, R. H., & Johns, E. H. (1975). An improved large scale fractionation of high mobility group nonhistone chromatin proteins. Biochim. Biophys. Acta 405:280.

    PubMed  Google Scholar 

  • Goodwin, G. H., Walker, J. M., & Johns, E. W. (1978). The high mobility group (HMG) nonhistone chromosomal proteins. In Busch, H. (ed.), The Cell Nucleus, Vol. 6, Academic Press, New York, pp. 182–217.

    Google Scholar 

  • Grasser, K. D. (1995). Plant chromosomal high mobility group HMG proteins. Plant J. 7:185.

    Article  PubMed  Google Scholar 

  • Grasser, K. D., Teo, S. H., Lee, K. B., Broadhurst, R. W., Rees, C., Hardman, C. H., & Thomas, J. O. (1998). DNA-binding properties of the tandem HMG boxes of high-mobility-group protein 1 (HMG1). Eur. J. Biochem. 253:787.

    PubMed  Google Scholar 

  • Grosschedl, R., Giese, K., & Pagel, J. (1992). HMG domain proteins: Architectural elements in the assembly of nucleoprotein structures. Trends Genet. 10:94.

    Google Scholar 

  • Heyduk, E., Heyduk, T., Claus, P., & Wisniewski, J. R. (1997). Conformational changes of DNA induced by binding of Chironomus high mobility group protein 1a: Regions flanking an HMG1–box domain do not influence the bend angle of the DNA. J. Biol. Chem. 272:19763.

    PubMed  Google Scholar 

  • Huth, J. R., Bewley, C. A., Nissen, M. S., Evans, J. N. S., Reeves, R., Gronenborn, A. M., & Clore, G. M. (1997). The solution structure of an HMGI(Y)-DNA complex defined a new architectural minor groove binding motif. Nat. Struct. Biol. 4:657.

    PubMed  Google Scholar 

  • Johns, E. W. (1964). Studies on histones. VII. Preparative methods for histone fractions from calf thymus. Biochem. J. 92:55.

    PubMed  Google Scholar 

  • Johns, E. W. (1982). The HMG Chromosomal Proteins, Academic Press, London.

    Google Scholar 

  • Jones, D. N., Searles, M. A., Shaw, G. L., Churchill, M. E., Ner, S. S., Keeler, J., Travers, A., & Neuhaus, D. (1994). The solution structure and dynamics of the DNA-binding domain of the HMG-D from Drosophila melanogaster. Structure 2:609.

    PubMed  Google Scholar 

  • Lehn, D. A., Elton, T. S., Johnson, K. R., & Reeves, R. (1988). A conformational study of the sequence specific binding of HMG-I (Y) with the bovine interleukin-2 cDNA. Biochem. Int. 16:963.

    PubMed  Google Scholar 

  • Levinger, L., & Varshavsky, A. (1982). Protein D1 preferentially binds Arich DNA in vitro and is a component of Drosophila melanogaster nucleosomes containing A rich satellite DNA. Proc. Natl. Acad. Sci. U.S.A. 79:7152.

    PubMed  Google Scholar 

  • Lnenicek-Allen, M., Read, C. M., & Crane-Robinson, C. (1996). The DNA bend angle and binding affinity of an HMG box increased by the presence of short terminal arms. Nucleic Acids Res. 24:1047.

    PubMed  Google Scholar 

  • Lovell-Badge, R. (1995). The HMG family of proteins. Nature 376:725.

    PubMed  Google Scholar 

  • Lund, T., Holtlund, J., Fredriksen, M., & Laland, S. G. (1983). On the presence of two new high mobility group like-proteins in HeLa S3 cells. FEBS Lett. 21:163.

    Google Scholar 

  • Lund, T., Skalhegg, B., Holtlund, J., Blomhoff, H. K., & Laland, S. G. (1987). Fractionation and identification of metaphase-specific phosphorylated forms of high-mobility-group proteins. Eur. J. Biochem. 166:21.

    PubMed  Google Scholar 

  • Maher, J. F., & Nathans, D. (1996). Multivalent DNA-binding properties of the HMG-I protein. Proc. Natl. Acad. Sci. U.S.A. 93:6716.

    PubMed  Google Scholar 

  • Mardian, J. K. W., Paton, A. E., Bunick, G. J., & Olins, D. E. (1980). Nucleosome cores have two specific binding sites for nonhistone chromosomal proteins HMG14 and HMG17. Science 209:1534.

    PubMed  Google Scholar 

  • Murphy, F. V., Sweet, R. M., & Churchill, M. E. (1999). The structure of the chromosomal high mobility group protein-DNA complex reveals sequence-neutral mechanisms important for non-sequence-specific DNA recognition. EMBO J. 18:6610.

    PubMed  Google Scholar 

  • Ner, S. S., Churchill, M. E. A., Searles, M. A., & Travers, A. A. (1993). DHMG-Z, a second HMG-1 related protein in Drosophila melanogaster. Nucleic Acids Res. 21:4369.

    PubMed  Google Scholar 

  • Ner, S. S., & Travers, A. A. (1994). HMG-D, the Drosophila melanogaster homologue of HMG1 protein, is associated with early embryonic chromatin in the absence of histone H1. EMBO J. 13:1817.

    PubMed  Google Scholar 

  • Ner, S. S., Blank, T., Perez-Paralle, M. L., Grigliatti, T. A., Becker, P. B., & Travers, A. A. (2001). HMG-D and histone H1 interplay during chromatin assembly and early embryogenesis. J. Biol. Chem. 276:37569.

    PubMed  Google Scholar 

  • Nicolas, F. J., Cayuela, M. L., Martinez-Argudo, I. M., Ruiz-Vasquez, R. M., & Murillo, F. J. (1996). High mobility group I(Y)-like DNA-binding domains on a bacterial transcription factor. Proc. Natl. Acad. Sci. U.S.A. 93:6881.

    PubMed  Google Scholar 

  • Nightingale, K., Dimitrov, S., Reeves, R., & Wolffe, A. P. (1996). Evidence for a shared structural role for HMG1 and linker histones B4 and H1 in organizing chromatin. EMBO J. 15:548.

    PubMed  Google Scholar 

  • Nissen, M. S., & Reeves, R. (1995). Changes in superhelicity are introduced into closed circular DNA by binding of high mobility group protein I/Y. J. Biol. Chem. 270:4355.

    PubMed  Google Scholar 

  • Paull, T., Haykinson, M. J., & Johnson, R. C. (1993). The nonspecific DNA-binding and bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev. 7:1521.

    PubMed  Google Scholar 

  • Payet, D., & Travers, A. (1997). The acidic tail of the high mobility group HMGD modulates the structural selectivity of DNA-binding. J. Mol. Biol. 266:66.

    PubMed  Google Scholar 

  • Payet, D., Hillisch, A., Lowe, N., Diekmann, S., & Travers, A. (1999). The recognition of distorted DNA structures by HMG-D: A footprinting and molecular modelling study. J. Mol. Biol. 294:79.

    PubMed  Google Scholar 

  • Piekielko, A., Drung, A., Rogalla, P., Schwanbeck, R., Heyduk, T., Gerharz, M., Bullerdiek, J., & Wisniewski, J. R. (2001). Distinct organization of DNA complexes of various HMGI/Y family proteins and their modulation upon mitotic phosphorylation. J. Biol. Chem. 276:1984.

    PubMed  Google Scholar 

  • Pontiggia, A., Rimini, R., Harley, V. R., Goodfellow, P. N., Lovell-Badge, R., & Bianchi, M. E. (1994). Sex-reversing mutations affect the architecture of SRY-DNA complexes. EMBO J. 13:6115.

    PubMed  Google Scholar 

  • Pontiggia, A., Whitfield, S., Goodfellow, P. N., Lovell-Badge, R., & Bianchi, M. E. (1995). Evolutionary conservation in the DNA-binding and bending properties of HMG-boxes from SRY proteins of primates. Gene 154:277.

    PubMed  Google Scholar 

  • Postinkov, Y. V., Trieschmann, L., Rickers, A., & Bustin, M. (1995). Homodimers of chromosomal proteins HMG-14 and 17 in nucleosome cores. J. Mol. Biol. 252:423.

    PubMed  Google Scholar 

  • Read, C. M., Cary P. D., Crane-Robinson, C., Driscoll, P. C., & Norman, D. G. (1993). Solution structure of a DNA-binding domain from HMG1. Nucleic Acids Res. 21:3427.

    PubMed  Google Scholar 

  • Reeves, R., & Beckerbauer, L. (2001). HMGI/Y proteins: Flexible regulators of transcription and chromatin structure. Biochim. Biophys. Acta 1519:13.

    PubMed  Google Scholar 

  • Reeves, R., & Nissen, M. S. (1990). The AT-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J. Biol. Chem. 265:8573.

    PubMed  Google Scholar 

  • Renner, U., Ghidelli, S., Schafer, M. A., & Wisniewski, J. R. (2000). Alterations in titer and distribution of high mobility group proteins during embryonic development of Drosophila melanogaster. Biochim. Biophys. Res. Commun. 1475:99.

    Google Scholar 

  • Rodriguez-Alfageme, C., Rudkin, G. T., & Cohen, L. (1980). Isolation properties and cellular distribution of D1, a chromosomal protein of Drosophila. Chromosoma 78:1.

    Article  PubMed  Google Scholar 

  • Sandeen, G., Wood, W. I., & Felsenfeld, G. (1980). The interaction of high mobility group proteins HMG 14 and 17 with nucleosomes. Nucleic Acids Res. 8:3757.

    PubMed  Google Scholar 

  • Sanders, C. (1977). A method for the fractionation of the high mobility group non histone chromosomal proteins. Biochem. Biophys. Res. Commun. 78:1034.

    PubMed  Google Scholar 

  • Schwanbeck, R., & Wisniewski, J. R. (1997). Cdc2 and mitogen-activated protein kinases modulate DNA-binding properties of the putative transcriptional regulator Chironomus high mobility group protein I. J. Biol. Chem. 272:27476

    PubMed  Google Scholar 

  • Schwanbeck, R., Manfioletti, G., & Wisniewski, J. R. (2000). Architecture of high mobility group protein I-C. DNA complex and its perturbation upon phosphorylation by Cdc 2 kinase. J. Biol. Chem. 275:1793.

    PubMed  Google Scholar 

  • Schwanbeck, R., Gymnopoulos, M., Petry, I., Piekielko, A., Szewczuk, Z., Heyduk, T., Zechel, K., & Wisniewski, J. R. (2001). Consecutive steps of phosphorylation affect conformation and DNA-binding of the Chironomus High Mobility Group A protein. J. Biol. Chem. 276:26012.

    PubMed  Google Scholar 

  • Shick, V. V., Belyavsky, A. V., & Mirzabekov, A. D. (1985). Primary organization of nucleosomes: Interaction of nonhistone high mobility group proteins 14 and 17 with nucleosomes, as revealed by DNA-protein crosslinking and immunoaffinity isolation. J. Mol. Biol. 185:329.

    PubMed  Google Scholar 

  • Shirakata, M. K., Huppi, S., Usuda, K., Yoshida, H., & Sakano, H. (1991). HMG1–related DNA-binding protein isolated with V-(D)-J recombination signal probes. Mol. Cell Biol. 11:4528.

    PubMed  Google Scholar 

  • Siegel, V., & Walter, P. (1988). Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: Analysis of biochemical mutants of SRP. Cell 52:39.

    Article  PubMed  Google Scholar 

  • Solomon, M. J., Straus, F., & Varshavsky, A. (1986). A mammalian high mobility group protein recognizes any stretch of six A.T base pairs in duplex DNA. Proc. Natl. Acad. Sci. U.S.A. 83:1276.

    PubMed  Google Scholar 

  • Spiker, S., Mardian, J. K. W., & Isenberg, I. (1978). Chromosomal HMG Proteins occur in three eucaryotic kingdoms. Biochem. Biophys. Res. Commun. 82:129.

    PubMed  Google Scholar 

  • Strauss, F., & Varshavsky, A. (1984). A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome. Cell 37:889.

    Article  PubMed  Google Scholar 

  • Stroumbakis, N. D., & Tolias, P. P. (1994). Localized maternal and zygotic expression of the gene encoding Drosophila HMGD. Biochim. Biophys. Acta 1218:245.

    PubMed  Google Scholar 

  • Teo, S. H., Grasser, K. D., & Thomas, J. O. (1995). Differences in the DNA-binding properties of the HMG-box domains of HMG1 and the sex-determining factor SRY. Eur. J. Biochem. 230:943.

    PubMed  Google Scholar 

  • Trieschmann, L., Postnikov, Y., Rickers, A., & Bustin, M. (1995). Modular structure of chromosomal proteins HMG-14/-17: Definition of a transcriptional activation domain distinct from the nucleosomal binding domain. Mol. Cell Biol. 15:6663.

    PubMed  Google Scholar 

  • Ura, K., Nightingale, K., & Wolffe, A. P. (1996). Differential association of HMG1 and linker histones B4 and H1 with dinucleosomal DNA: Structural transitions and transcriptional repression. EMBO J. 15:4959.

    PubMed  Google Scholar 

  • Wagner, C. R., Hamana, K., & Elgin, S. C. R. (1992). A high mobility group protein and its cDNA from Drosophila melanogaster. Mol. Cell Biol. 12:1915.

    PubMed  Google Scholar 

  • Wang, D. Z., Ray, P., & Boothby, M. (1995). Interleukin 4–inducible phosphorylation of HMG-I(Y) is inhibited by rapamycin. J. Biol. Chem. 270:22924.

    PubMed  Google Scholar 

  • Wang, D., Zamorano, J., Keegan, A. D., & Boothby, M. (1997). HMG-I(Y) phosphorylation status as a nuclear target regulated through insulin receptor substrate-1 and the 14R motif of the interleukin-4 receptor. J. Biol. Chem. 272:25083.

    PubMed  Google Scholar 

  • Watson, D. C., Peters, E. M., & Dixon, G. H. (1977). The purification, characterization and partial sequence determination of a trout testis nonhistone protein, HMG-T. Eur. J. Biochem. 74:53.

    PubMed  Google Scholar 

  • Weber, S., & Isenberg, I. (1980). High mobility group proteins of Saccharomyces cerevisiae. Biochemistry 19:2236.

    PubMed  Google Scholar 

  • Weir, H. M., Kraulis, P. J., Hill, C. S., Raine, R. C., Laue, E. D., & Thomas, J. O. (1993). Structure of the HMG box motif in the B-domain of the HMG1. EMBO J. 12:1311.

    PubMed  Google Scholar 

  • Werner, M. H., Huth, J. R., Gronenborn, A. M., & Clore, G. M. (1995). Molecular basis of human 46 X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell 81:705.

    PubMed  Google Scholar 

  • Wisniewski, J. R., & Schulze, E. (1992). Insect proteins homologous to mammalian high mobility group proteins 1: Characterization and DNA-binding properties. J. Biol. Chem. 267:17170.

    PubMed  Google Scholar 

  • Wisniewski, J. R., & Schulze, E. (1994). High affinity interaction of dipteran high mobility (HMG) group proteins 1 with DNA is modulated by COOH-terminal regions flanking the HMG Box Domain. J. Biol. Chem. 269:10713.

    PubMed  Google Scholar 

  • Wisniewski, J. R., Schulze, E., & Sapetto, B. (1994). DNA-binding and nuclear translocation of insect high-mobility-group-protein-1 (HMG1) proteins are inhibited by phosphorylation. Eur. J. Biochem. 255:687.

    Google Scholar 

  • Wisniewski, J. R., Hessler, K., Claus, P., & Zechel, K. (1997). Structural and functional consequences of mutations within the hydrophobic cores of the HMG1–box domain of the Chironomus high mobility group protein 1a. Eur. J. Biochem. 243:151.

    PubMed  Google Scholar 

  • Xiao, D. M., Pak, J. H., Wang, X., Sato, T., Huang, F. L., Chen, H. C., & Huang, K. P. (2000). Phosphorylation of HMG-I by protein kinase C attenuates its binding affinity to the promoter regions of protein kinase C gamma and neurogranin/RC3 genes. J. Neurochem. 74:392.

    PubMed  Google Scholar 

  • Yie, J., Liang, S., Merika, M., & Thanos, D. (1997). Intra-and intermolecular cooperative binding of high-mobility-group protein I(Y) to the beta-interferon promoter. Mol. Cell Biol. 17:3649.

    PubMed  Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aleporou-Marinou, V., Marinou, H. & Patargias, T. A Mini Review of the High Mobility Group Proteins of Insects. Biochem Genet 41, 291–304 (2003). https://doi.org/10.1023/B:BIGI.0000006030.05308.04

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:BIGI.0000006030.05308.04

Navigation