Sequence Profile of the Parallel β Helix in the Pectate Lyase Superfamily

The parallel β helix structure found in the pectate lyase superfamily has been analyzed in detail. A comparative analysis of known structures has revealed a unique sequence profile, with a strong positional preference for specific amino acids oriented toward the interior of the parallel β helix. Using the unique sequence profile, search patterns have been constructed and applied to the sequence databases to identify a subset of proteins that are likely to fold into the parallel β helix. Of the 19 families identified, 39% are known to be carbohydrate-binding proteins, and 50% belong to a broad category of proteins with sequences containing leucine-rich repeats (LRRs). The most striking result is the sequence match between the search pattern and four contiguous segments of internalin A, a surface protein from the bacterial pathogenListeria monocytogenes.A plausible model of the repetitive LRR sequences of internalin A has been constructed and favorable 3D–1D profile scores have been calculated. Moreover, spectroscopic features characteristic of the parallel β helix topology in the pectate lyases are present in the circular dichroic spectrum of internalin A. Altogether, the data support the hypothesis that sequence search patterns can be used to identify proteins, including a subset of LRR proteins, that are likely to fold into the parallel β helix.

[1]  S. Wodak,et al.  Modeling of the three-dimensional structure of proteins with the typical leucine-rich repeats. , 1995, Structure.

[2]  R Nussinov,et al.  Fast protein fold recognition via sequence to structure alignment and contact capacity potentials. , 1996, Pacific Symposium on Biocomputing. Pacific Symposium on Biocomputing.

[3]  Douglas C. Rees,et al.  A leucine-rich repeat variant with a novel repetitive protein structural motif , 1996, Nature Structural Biology.

[4]  D. Eisenberg,et al.  Assessment of protein models with three-dimensional profiles , 1992, Nature.

[5]  M. Yoder,et al.  New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. , 1993, Science.

[6]  E. Estabrook,et al.  Plant-Plant Communications: Rhizosphere Signaling between Parasitic Angiosperms and Their Hosts , 1998 .

[7]  N. Kestner.  Electrons in liquid ammonia , 1977, Nature.

[8]  Bostjan Kobe,et al.  Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats , 1993, Nature.

[9]  M. Yoder,et al.  The Refined Three-Dimensional Structure of Pectate Lyase C from Erwinia chrysanthemi at 2.2 Angstrom Resolution (Implications for an Enzymatic Mechanism) , 1995, Plant physiology.

[10]  P. Cossart,et al.  Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci , 1991, Cell.

[11]  M. Yoder,et al.  The parallel β helix and other coiled folds , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[12]  L. Banaszak,et al.  Structure and function of a lipoprotein: lipovitellin. , 1991, Annual review of biophysics and biophysical chemistry.

[13]  M. Yoder,et al.  The Three-Dimensional Structure of Pectate Lyase E, a Plant Virulence Factor from Erwinia chrysanthemi , 1994, Plant physiology.

[14]  H. Edelhoch,et al.  Spectroscopic determination of tryptophan and tyrosine in proteins. , 1967, Biochemistry.

[15]  C. Chothia,et al.  Structural patterns in globular proteins , 1976, Nature.

[16]  C. Raetz,et al.  A Left-Handed Parallel β Helix in the Structure of UDP-N-Acetylglucosamine Acyltransferase , 1995, Science.

[17]  W C Johnson,et al.  Protein secondary structure and circular dichroism: A practical guide , 1990, Proteins.

[18]  M. Yoder,et al.  The Refined Three-Dimensional Structure of Pectate Lyase E from Erwinia chrysanthemi at 2.2 A Resolution , 1996, Plant physiology.

[19]  A. Brunger.  Crystallographic refinement by simulated annealing , 1988 .

[20]  O. Mayans,et al.  Two crystal structures of pectin lyase A from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases. , 1997, Structure.

[21]  P. Emsley,et al.  Structure of Bordetella pertussis virulence factor P.69 pertactin , 1996, Nature.

[22]  S. Steinbacher,et al.  Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. , 1994, Science.

[23]  F. Jurnak,et al.  Circular dichroism of the parallel β helical proteins pectate lyase C and E , 1995 .

[24]  H. Schindelin,et al.  A left‐hand beta‐helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila. , 1996, The EMBO journal.

[25]  J. Richardson,et al.  The anatomy and taxonomy of protein structure. , 1981, Advances in protein chemistry.

[26]  M. Yoder,et al.  Unusual structural features in the parallel β-helix in pectate lyases , 1993 .

[27]  P. Cossart,et al.  Antibodies to the leucine-rich repeat region of internalin block entry of Listeria monocytogenes into cells expressing E-cadherin , 1996, Infection and immunity.

[28]  J. Thornton,et al.  PROCHECK: a program to check the stereochemical quality of protein structures , 1993 .

[29]  B Henrissat,et al.  Functional Implications of Structure-Based Sequence Alignment of Proteins in the Extracellular Pectate Lyase Superfamily , 1995, Plant physiology.

[30]  R. Pickersgill,et al.  The structure of Bacillus subtilis pectate lyase in complex with calcium , 1994, Nature Structural Biology.

[31]  J M Thornton,et al.  Successful protein fold recognition by optimal sequence threading validated by rigorous blind testing , 1995, Proteins.

[32]  S. Kauppinen,et al.  The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel beta helix. , 1997, Structure.

[33]  U. Baumann,et al.  Three‐dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two‐domain protein with a calcium binding parallel beta roll motif. , 1993, The EMBO journal.

[34]  P. Cossart,et al.  E-Cadherin Is the Receptor for Internalin, a Surface Protein Required for Entry of L. monocytogenes into Epithelial Cells , 1996, Cell.

[35]  J. Visser,et al.  The tree-dimensional structure of aspergillus niger pectin lyase B at 1.7-A resolution. , 1998, Plant physiology.

[36]  J. Deisenhofer,et al.  The leucine-rich repeat: a versatile binding motif. , 1994, Trends in biochemical sciences.

[37]  N. Gay,et al.  Structural and functional diversity in the leucine-rich repeat family of proteins. , 1996, Progress in biophysics and molecular biology.

[38]  D Eisenberg,et al.  A 3D-1D substitution matrix for protein fold recognition that includes predicted secondary structure of the sequence. , 1997, Journal of molecular biology.