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Difference between revisions of "Glycoside Hydrolase Family 35"

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== Substrate specificities ==
 
== Substrate specificities ==
The majority of GH35 members are β-galactosidases (EC [{{EClink}}3.2.1.23 3.2.1.23]).  GH35 enzymes have been isolated from microorganisms such as fungi, bacteria and yeasts, as well as higher organisms such as plants, animals, and human cells.  These β-galactosidases catalyse the hydrolysis of terminal non-reducing β-D-galactose residues in, for example, lactose (1,4-O-β-D-galactopyranosyl-D-glucose), oligosaccharides, glycolipids, and glycoproteins. Various GH35 β-galactosidases demonstrate specificity towards β1,3-, β1,6- or  β1,4-galactosidic linkages '''(REFS NEEDED)''', and are often most active under acidic conditions '''(REFS NEEDED)'''.  As with many other CAZy families <cite>GeislerLee2006, Henrissat2001, Tuskan2006</cite>, GH35 members tend to be represented by multi-gene families in plants <cite>Ahn2007, Smith2000, Lazan2004, Ross1994, Tanthanuch2008</cite>. Moreover, plant GH35 β-galactosidases have be divided into two classes: members of the first are capable of hydrolyzing pectic β-1,4-galactans, while those of the second can specifically cleave β-1,3- and β1,6-galactosyl linkages of arabinogalactan proteins '''(REFS NEEDED)'''.
+
The majority of GH35 members are β-galactosidases (EC [{{EClink}}3.2.1.23 3.2.1.23]).  GH35 enzymes have been isolated from microorganisms such as fungi, bacteria and yeasts, as well as higher organisms such as plants, animals, and human cells.  These β-galactosidases catalyse the hydrolysis of terminal non-reducing β-D-galactose residues in, for example, lactose (1,4-O-β-D-galactopyranosyl-D-glucose), oligosaccharides, glycolipids, and glycoproteins. Various GH35 β-galactosidases demonstrate specificity towards β1,3-, β1,6- or  β1,4-galactosidic linkages <cite>Zinin2002, Gamauf2007, Tanthanuch2008</cite>, and are often most active under acidic conditions <cite>Zhang1994, van Casteren2000, Wang2009</cite>.  As with many other CAZy families <cite>GeislerLee2006, Henrissat2001, Tuskan2006</cite>, GH35 members tend to be represented by multi-gene families in plants <cite>Ahn2007, Smith2000, Lazan2004, Ross1994, Tanthanuch2008</cite>. Moreover, plant GH35 β-galactosidases have be divided into two classes: members of the first are capable of hydrolyzing pectic β-1,4-galactans, while those of the second can specifically cleave β-1,3- and β1,6-galactosyl linkages of arabinogalactan proteins <cite>Kotake2005</cite>.
  
In addition to β-galactosidases, GH35 also contains a limited number of archeal exo-β-glucosaminidases (EC [{{EClink}}3.2.1.165 3.2.1.165]) <cite>Tanaka2003 Kawarabayasi1998</cite> '''(NEED ORIGINAL BIOCHEMICAL REF FOR PYROCCOCCUS ENZYME; NOT GENOME PAPER)'''. Such enzymes hydrolyze chitosan or chitosan oligosaccharides to remove successive D-glucosamine residues from non-reducing termini.
+
In addition to β-galactosidases, GH35 also contains a limited number of archeal exo-β-glucosaminidases (EC [{{EClink}}3.2.1.165 3.2.1.165]) <cite>Tanaka2003 Liu2006</cite>. Such enzymes hydrolyze chitosan or chitosan oligosaccharides to remove successive D-glucosamine residues from non-reducing termini.
  
 
== Kinetics and Mechanism ==
 
== Kinetics and Mechanism ==
Beta-galactosidases of GH35 catalyze the hydrolysis of terminal β-galactosyl residues via a double-displacement mechanism, which leads to net retention of the β-anomeric configuration of the released galactose molecule. The stereochemistry of the reaction was first shown by NMR for the human β-galactosidase precursor <cite>Zhang1994</cite> and has been subsequently confirmed by other investigators for microbial and plant enzymes '''(REFS NEEDED)'''.
+
Beta-galactosidases of GH35 catalyze the hydrolysis of terminal β-galactosyl residues via a double-displacement mechanism, which leads to net retention of the β-anomeric configuration of the released galactose molecule. The stereochemistry of the reaction was first shown by NMR for the human β-galactosidase precursor <cite>Zhang1994</cite> and has been subsequently confirmed by other investigators for microbial and plant enzymes <cite>Casteren2000, Zinin2002</cite> .
  
 
== Catalytic Residues ==
 
== Catalytic Residues ==
The catalytic residues for family 35 were first predicted on the basis of hydrophobic cluster analysis of proteins of similar protein fold <cite>Henrissat1995</cite>. Experimentally, the glutamic acid residue 268 was first identified as the catalytic nucleophile in human lysosomal β-galactosidase precursor using a slow substrate, 2,4-dinitrophenyl-2-deoxy-2-fluoro- β-D-galactopyranoside, that allowed trapping of a covalent glycosyl-enzyme intermediate. This allowed subsequent peptide mapping to exactly identify the catalytic nucleophile <cite>McCarter</cite>. Subsequently, this approach was repeated for two bacterial β-galactosidases from ''Xanthomonas manihotis'' and ''Bacillus circulans'' <cite>Blanchard2001</cite>. The general acid/base catalyst was inferred to be  Glu200 from structural studies of a ''Penicillium'' sp. β-galactosidase <cite>Rojas2004</cite>. Recent structural studies <cite>Maksimainen2010</cite> revealed two different conformations of the general acid/base catalyst in the β-galactosidase of ''Trichoderma reesei''.
+
The catalytic residues for family 35 were first predicted on the basis of hydrophobic cluster analysis of proteins of similar protein fold <cite>Henrissat1995</cite>. Experimentally, the glutamic acid residue 268 was first identified as the catalytic nucleophile in human lysosomal β-galactosidase precursor using a slow substrate, 2,4-dinitrophenyl-2-deoxy-2-fluoro- β-D-galactopyranoside, that allowed trapping of a covalent glycosyl-enzyme intermediate. This allowed subsequent peptide mapping to exactly identify the catalytic nucleophile <cite>McCarter1997</cite>. Subsequently, this approach was repeated for two bacterial β-galactosidases from ''Xanthomonas manihotis'' and ''Bacillus circulans'' <cite>Blanchard2001</cite>. The general acid/base catalyst was inferred to be  Glu200 from structural studies of a ''Penicillium'' sp. β-galactosidase <cite>Rojas2004</cite>. Recent structural studies <cite>Maksimainen2010</cite> revealed two different conformations of the general acid/base catalyst in the β-galactosidase of ''Trichoderma reesei''.
  
 
== Three-dimensional structures ==
 
== Three-dimensional structures ==
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#Tanthanuch2008 pmid=18664295
 
#Tanthanuch2008 pmid=18664295
 
#Tanka2003 pmid=12923090
 
#Tanka2003 pmid=12923090
#Kawarabayasi1998 pmid=9679203
+
#Liu2006 pmid=16912928
 
#Zhang1994 pmid=7998946
 
#Zhang1994 pmid=7998946
 
#Henrissat1995 pmid=7624375
 
#Henrissat1995 pmid=7624375
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#Henrissat2001 pmid=11554480
 
#Henrissat2001 pmid=11554480
 
#Tuskan2006 pmid=16973872
 
#Tuskan2006 pmid=16973872
 +
#Gamauf2007 pmid=17381511
 +
#Zinin2002 pmid=11909597
 +
#van Casteren2000 pmid=11086688
 +
#Wang2009 pmid=19453169
 +
#Kotake2005 pmid=15980190
 
</biblio>
 
</biblio>
  
  
 
[[Category:Glycoside Hydrolase Families|GH035]]
 
[[Category:Glycoside Hydrolase Families|GH035]]

Revision as of 05:50, 8 February 2011

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Glycoside Hydrolase Family GH35
Clan GH-A
Mechanism retaining
Active site residues known
CAZy DB link
https://www.cazy.org/GH35.html


Substrate specificities

The majority of GH35 members are β-galactosidases (EC 3.2.1.23). GH35 enzymes have been isolated from microorganisms such as fungi, bacteria and yeasts, as well as higher organisms such as plants, animals, and human cells. These β-galactosidases catalyse the hydrolysis of terminal non-reducing β-D-galactose residues in, for example, lactose (1,4-O-β-D-galactopyranosyl-D-glucose), oligosaccharides, glycolipids, and glycoproteins. Various GH35 β-galactosidases demonstrate specificity towards β1,3-, β1,6- or β1,4-galactosidic linkages [1, 2, 3], and are often most active under acidic conditions [4, 5, 6, 7]. As with many other CAZy families [8, 9, 10], GH35 members tend to be represented by multi-gene families in plants [3, 11, 12, 13, 14]. Moreover, plant GH35 β-galactosidases have be divided into two classes: members of the first are capable of hydrolyzing pectic β-1,4-galactans, while those of the second can specifically cleave β-1,3- and β1,6-galactosyl linkages of arabinogalactan proteins [15].

In addition to β-galactosidases, GH35 also contains a limited number of archeal exo-β-glucosaminidases (EC 3.2.1.165) [16, 17]. Such enzymes hydrolyze chitosan or chitosan oligosaccharides to remove successive D-glucosamine residues from non-reducing termini.

Kinetics and Mechanism

Beta-galactosidases of GH35 catalyze the hydrolysis of terminal β-galactosyl residues via a double-displacement mechanism, which leads to net retention of the β-anomeric configuration of the released galactose molecule. The stereochemistry of the reaction was first shown by NMR for the human β-galactosidase precursor [4] and has been subsequently confirmed by other investigators for microbial and plant enzymes [1, 6] .

Catalytic Residues

The catalytic residues for family 35 were first predicted on the basis of hydrophobic cluster analysis of proteins of similar protein fold [18]. Experimentally, the glutamic acid residue 268 was first identified as the catalytic nucleophile in human lysosomal β-galactosidase precursor using a slow substrate, 2,4-dinitrophenyl-2-deoxy-2-fluoro- β-D-galactopyranoside, that allowed trapping of a covalent glycosyl-enzyme intermediate. This allowed subsequent peptide mapping to exactly identify the catalytic nucleophile [19]. Subsequently, this approach was repeated for two bacterial β-galactosidases from Xanthomonas manihotis and Bacillus circulans [20]. The general acid/base catalyst was inferred to be Glu200 from structural studies of a Penicillium sp. β-galactosidase [21]. Recent structural studies [22] revealed two different conformations of the general acid/base catalyst in the β-galactosidase of Trichoderma reesei.

Three-dimensional structures

As of February 2011, only three enzymes from GH35 have been structurally characterized. The first 3D-structures of a GH35 enzyme, those of a β-galactosidase from Pencillium sp. (Psp-β-gal) in native (PDB 1tg7) and product-complexed (PDB 1xc6) forms, were reported in 2004 at 1.90 Å and 2.10 Å resolution, respectively [21]. The structure of a β-galactosidase from Bacteriodes thetaiotamicron was subsequently reported by the New York Structural GenomiX Research Consortium in 2008 at 2.15 Å resolution (PDB 3d3a). In 2010, a high (1.2 Å) resolution crystal structure of a Trichoderma reesei (Hypocrea jecorina) β-galactosidase (Tr-β-gal, PDB 3og2) was reported, together with complex structures with galactose, IPTG and PETG at 1.5, 1.75 and 1.4 Å resolutions, respectively (PDB codes 3ogr, 3ogs, and 3ogv, respectively) [22].

GH35 enzymes belong to Clan GH-A, and thus have a (α/β)8 TIM barrel comprising the catalytic domain. A structural analysis of the galactose-binding active-site was based on the comparison of the crystallographic models of the native Psp-β-gal and Tr-β-gal enzymes and their respective complexes with galactose. A single galactose molecule is bound to the TIM barrel domain of the enzyme in the chair conformation in the β-anomeric configuration. Two glutamic acid residues act as the general acid-base and nucleophilic catalysts; these are presented on strands 4 and 7 of the barrel. Although the crystal structures of Psp-β-gal and Tr-β-gal are similar, interpretation of the structure of Tr-β-gal is somewhat different from that presented earlier for Psp-β-gal: Rojas et al. considered Psp-β-gal to be divided into five domains combining the second and the third domain, although they form separate sub-units in the structure [21]. In contrast, Maksimainen et al. concluded that the Tr-β-gal structure contains a central catalytic α/β-barrel surrounded by a horseshoe consisting of five anti-parallel β-sandwich structures [22].

Additionally, Maksimainen et al. have described conformational changes in two loop regions of the active site of Tr-β-gal, thus implicating a conformational selection mechanism for the enzyme. The acid/base catalyst Glu200 exhibited two different conformations which affect the pKa value of this residue and thus the catalytic mechanism.

Family Firsts

First stereochemistry determination

Human β-galactosidase precursor by NMR [4]

First catalytic nucleophile identification

Human β-galactosidase precursor by 2-fluorogalactose labeling [19].

First general acid/base residue identification

Penicillium sp. β-galactosidase by structural identification [21].

First 3-D structure

Penicillium sp. β-galactosidase [21].

References

  1. Zinin AI, Eneyskaya EV, Shabalin KA, Kulminskaya AA, Shishlyannikov SM, and Neustroev KN. (2002). 1-O-Acetyl-beta-D-galactopyranose: a novel substrate for the transglycosylation reaction catalyzed by the beta-galactosidase from Penicillium sp. Carbohydr Res. 2002;337(7):635-42. DOI:10.1016/s0008-6215(02)00027-7 | PubMed ID:11909597 [Zinin2002]
  2. Gamauf C, Marchetti M, Kallio J, Puranen T, Vehmaanperä J, Allmaier G, Kubicek CP, and Seiboth B. (2007). Characterization of the bga1-encoded glycoside hydrolase family 35 beta-galactosidase of Hypocrea jecorina with galacto-beta-D-galactanase activity. FEBS J. 2007;274(7):1691-700. DOI:10.1111/j.1742-4658.2007.05714.x | PubMed ID:17381511 [Gamauf2007]
  3. Tanthanuch W, Chantarangsee M, Maneesan J, and Ketudat-Cairns J. (2008). Genomic and expression analysis of glycosyl hydrolase family 35 genes from rice (Oryza sativa L.). BMC Plant Biol. 2008;8:84. DOI:10.1186/1471-2229-8-84 | PubMed ID:18664295 [Tanthanuch2008]
  4. Zhang S, McCarter JD, Okamura-Oho Y, Yaghi F, Hinek A, Withers SG, and Callahan JW. (1994). Kinetic mechanism and characterization of human beta-galactosidase precursor secreted by permanently transfected Chinese hamster ovary cells. Biochem J. 1994;304 ( Pt 1)(Pt 1):281-8. DOI:10.1042/bj3040281 | PubMed ID:7998946 [Zhang1994]
  5. Casteren2000 pmid=11086688

    [van]
  6. Wang H, Luo H, Bai Y, Wang Y, Yang P, Shi P, Zhang W, Fan Y, and Yao B. (2009). An acidophilic beta-galactosidase from Bispora sp. MEY-1 with high lactose hydrolytic activity under simulated gastric conditions. J Agric Food Chem. 2009;57(12):5535-41. DOI:10.1021/jf900369e | PubMed ID:19453169 [Wang2009]
  7. Geisler-Lee J, Geisler M, Coutinho PM, Segerman B, Nishikubo N, Takahashi J, Aspeborg H, Djerbi S, Master E, Andersson-Gunnerås S, Sundberg B, Karpinski S, Teeri TT, Kleczkowski LA, Henrissat B, and Mellerowicz EJ. (2006). Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol. 2006;140(3):946-62. DOI:10.1104/pp.105.072652 | PubMed ID:16415215 [GeislerLee2006]
  8. Henrissat B, Coutinho PM, and Davies GJ. (2001). A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol Biol. 2001;47(1-2):55-72. | Google Books | Open Library PubMed ID:11554480 [Henrissat2001]
  9. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, and Rokhsar D. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006;313(5793):1596-604. DOI:10.1126/science.1128691 | PubMed ID:16973872 [Tuskan2006]
  10. Ahn YO, Zheng M, Bevan DR, Esen A, Shiu SH, Benson J, Peng HP, Miller JT, Cheng CL, Poulton JE, and Shih MC. (2007). Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry. 2007;68(11):1510-20. DOI:10.1016/j.phytochem.2007.03.021 | PubMed ID:17466346 [Ahn2007]
  11. Smith DL and Gross KC. (2000). A family of at least seven beta-galactosidase genes is expressed during tomato fruit development. Plant Physiol. 2000;123(3):1173-83. DOI:10.1104/pp.123.3.1173 | PubMed ID:10889266 [Smith2000]
  12. Lazan H, Ng SY, Goh LY, and Ali ZM. (2004). Papaya beta-galactosidase/galactanase isoforms in differential cell wall hydrolysis and fruit softening during ripening. Plant Physiol Biochem. 2004;42(11):847-53. DOI:10.1016/j.plaphy.2004.10.007 | PubMed ID:15694277 [Lazan2004]
  13. Ross GS, Wegrzyn T, MacRae EA, and Redgwell RJ. (1994). Apple beta-galactosidase. Activity against cell wall polysaccharides and characterization of a related cDNA clone. Plant Physiol. 1994;106(2):521-8. DOI:10.1104/pp.106.2.521 | PubMed ID:7991682 [Ross1994]
  14. Kotake T, Dina S, Konishi T, Kaneko S, Igarashi K, Samejima M, Watanabe Y, Kimura K, and Tsumuraya Y. (2005). Molecular cloning of a {beta}-galactosidase from radish that specifically hydrolyzes {beta}-(1->3)- and {beta}-(1->6)-galactosyl residues of Arabinogalactan protein. Plant Physiol. 2005;138(3):1563-76. DOI:10.1104/pp.105.062562 | PubMed ID:15980190 [Kotake2005]
  15. Liu B, Li Z, Hong Y, Ni J, Sheng D, and Shen Y. (2006). Cloning, expression and characterization of a thermostable exo-beta-D-glucosaminidase from the hyperthermophilic archaeon Pyrococcus horikoshii. Biotechnol Lett. 2006;28(20):1655-60. DOI:10.1007/s10529-006-9137-0 | PubMed ID:16912928 [Liu2006]
  16. Henrissat B, Callebaut I, Fabrega S, Lehn P, Mornon JP, and Davies G. (1995). Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc Natl Acad Sci U S A. 1995;92(15):7090-4. DOI:10.1073/pnas.92.15.7090 | PubMed ID:7624375 [Henrissat1995]
  17. McCarter JD, Burgoyne DL, Miao S, Zhang S, Callahan JW, and Withers SG. (1997). Identification of Glu-268 as the catalytic nucleophile of human lysosomal beta-galactosidase precursor by mass spectrometry. J Biol Chem. 1997;272(1):396-400. DOI:10.1074/jbc.272.1.396 | PubMed ID:8995274 [McCarter1997]
  18. Blanchard JE, Gal L, He S, Foisy J, Warren RA, and Withers SG. (2001). The identification of the catalytic nucleophiles of two beta-galactosidases from glycoside hydrolase family 35. Carbohydr Res. 2001;333(1):7-17. DOI:10.1016/s0008-6215(01)00108-2 | PubMed ID:11423106 [Blanchard2001]
  19. Rojas AL, Nagem RA, Neustroev KN, Arand M, Adamska M, Eneyskaya EV, Kulminskaya AA, Garratt RC, Golubev AM, and Polikarpov I. (2004). Crystal structures of beta-galactosidase from Penicillium sp. and its complex with galactose. J Mol Biol. 2004;343(5):1281-92. DOI:10.1016/j.jmb.2004.09.012 | PubMed ID:15491613 [Rojas2004]
  20. Maksimainen M, Hakulinen N, Kallio JM, Timoharju T, Turunen O, Rouvinen J. Crystal structures of Trichoderma reesei beta-galactosidase reveal conformational changes in the active site. J Struct Biol. 2010, in press.

    [Maksimainen2010]

    Note: Due to a problem with PubMed data, this reference is not automatically formatted. Please see these links out: DOI:10.1016/j.jsb.2010.11.024 PMID:21130883

  21. Tanaka T, Fukui T, Atomi H, and Imanaka T. (2003). Characterization of an exo-beta-D-glucosaminidase involved in a novel chitinolytic pathway from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol. 2003;185(17):5175-81. DOI:10.1128/JB.185.17.5175-5181.2003 | PubMed ID:12923090 [Tanka2003]

All Medline abstracts: PubMed