A Novel Putative Insect Chitinase with Multiple Catalytic Domains: Hormonal Regulation During Metamorphosis

Overview

Journal Biochem J

Specialty Biochemistry

Date 2002 Jun 13

PMID 12059786

Citations 15

Authors

Veronique Royer

Stephane Fraichard

Herve Bouhin

Affiliations

Soon will be listed here.

Abstract

We have used differential display to identify genes that are regulated by juvenile hormone in the epidermis of the beetle Tenebrio molitor. One of the genes encodes T. molitor chitinase 5 (TmChit5), a chitinase possessing an unusual structure. Sequence analysis of TmChit5 identified five 'chitinase units' of approx. 480 amino acids with similarity to chitinase family 18. These units are separated by less conserved regions containing putative PEST (rich in proline, glutamic acid, serine and threonine) sequences, putative chitin-binding domains and mucin domains. Northern-blot analysis identified a single transcript of approx. 9 kb, whose abundance correlated with that of 20-hydroxyecdysone during metamorphosis. Injection of pupae with 20-hydroxyecdysone alone, or in combination with cycloheximide, indicated that TmChit5 expression is directly induced by the hormone. Further experiments indicated that methoprene (a juvenile hormone analogue) indirectly induced TmChit5 mRNA expression. On the basis of the present results and previous studies, we propose a molecular mechanism for cuticle digestion during the moulting process.

Citing Articles

Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, (Coleoptera: Scolytinae).

Ashraf M, Mogilicherla K, Sellamuthu G, Siino V, Levander F, Roy A Front Plant Sci. 2023; 14:1157455.

PMID: 38078109 PMC: 10703158. DOI: 10.3389/fpls.2023.1157455.

An overview of viral chitinases: General properties and biotechnological potential.

Goncalves de Oliveira E, Filho C, Rodrigues R Exp Biol Med (Maywood). 2023; 248(22):2053-2061.

PMID: 38057942 PMC: 10800131. DOI: 10.1177/15353702231208408.

Effects of abiotic stresses on the expression of chitinase-like genes in .

Li C, Ul Haq I, Khurshid A, Tao Y, Quandahor P, Zhou J Front Physiol. 2022; 13:1024136.

PMID: 36505077 PMC: 9727142. DOI: 10.3389/fphys.2022.1024136.

Hexapod Assassins' Potion: Venom Composition and Bioactivity from the Eurasian Assassin Bug .

Rugen N, Jenkins T, Wielsch N, Vogel H, Hempel B, Sussmuth R Biomedicines. 2021; 9(7).

PMID: 34356883 PMC: 8301361. DOI: 10.3390/biomedicines9070819.

Structural dissection reveals a general mechanistic principle for group II chitinase (ChtII) inhibition.

Chen W, Zhou Y, Yang Q J Biol Chem. 2019; 294(24):9358-9364.

PMID: 31053640 PMC: 6579453. DOI: 10.1074/jbc.RA119.007812.

References

Dubrovsky E, Dubrovskaya V, Bilderback A, Berger E . The isolation of two juvenile hormone-inducible genes in Drosophila melanogaster. Dev Biol. 2000; 224(2):486-95. DOI: 10.1006/dbio.2000.9800. View

Nicolai M, Bouhin H, Quennedey B, Delachambre J . Molecular cloning and expression of Tenebrio molitor ultraspiracle during metamorphosis and in vivo induction of its phosphorylation by 20-hydroxyecdysone. Insect Mol Biol. 2000; 9(3):241-9. DOI: 10.1046/j.1365-2583.2000.00181.x. View

Riddiford L . Hormonal control of insect epidermal cell commitment in vitro. Nature. 1976; 259(5539):115-7. DOI: 10.1038/259115a0. View

Delbecque J, Hirn M, Delachambre J, De Regg M . Cuticular cycle and molting hormone levels during the metamorphosis of Tenebrio molitor (Insecta Coleoptera). Dev Biol. 1978; 64(1):11-30. DOI: 10.1016/0012-1606(78)90057-x. View

Fukamizo T, Kramer K, Mueller D, Schaefer J, Garbow J, Jacob G . Analysis of chitin structure by nuclear magnetic resonance spectroscopy and chitinolytic enzyme digestion. Arch Biochem Biophys. 1986; 249(1):15-26. DOI: 10.1016/0003-9861(86)90555-2. View

Rogers S, Wells R, Rechsteiner M . Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986; 234(4774):364-8. DOI: 10.1126/science.2876518. View

Brydon L, Gooday G, Chappell L, King T . Chitin in egg shells of Onchocerca gibsoni and Onchocerca volvulus. Mol Biochem Parasitol. 1987; 25(3):267-72. DOI: 10.1016/0166-6851(87)90090-9. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Higgins D, Sharp P . CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988; 73(1):237-44. DOI: 10.1016/0378-1119(88)90330-7. View

10.

Bouhin H, Charles J, Quennedey B, Delachambre J . Developmental profiles of epidermal mRNAs during the pupal-adult molt of Tenebrio molitor and isolation of a cDNA clone encoding an adult cuticular protein: effects of a juvenile hormone analogue. Dev Biol. 1992; 149(1):112-22. DOI: 10.1016/0012-1606(92)90268-l. View

11.

Liang P, Pardee A . Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992; 257(5072):967-71. DOI: 10.1126/science.1354393. View

12.

Gum Jr J, Hicks J, Toribara N, Rothe E, Lagace R, Kim Y . The human MUC2 intestinal mucin has cysteine-rich subdomains located both upstream and downstream of its central repetitive region. J Biol Chem. 1992; 267(30):21375-83. View

13.

Liang P, Averboukh L, Pardee A . Distribution and cloning of eukaryotic mRNAs by means of differential display: refinements and optimization. Nucleic Acids Res. 1993; 21(14):3269-75. PMC: 309766. DOI: 10.1093/nar/21.14.3269. View

14.

Henrissat B, Bairoch A . New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1993; 293 ( Pt 3):781-8. PMC: 1134435. DOI: 10.1042/bj2930781. View

15.

Celano P, Vertino P, Casero Jr R . Isolation of polyadenylated RNA from cultured cells and intact tissues. Biotechniques. 1993; 15(1):26-8. View

16.

Jones G, Venkataraman V, Manczak M . Transcriptional regulation of an unusual trypsin-related protein expressed during insect metamorphosis. Insect Biochem Mol Biol. 1993; 23(7):825-9. DOI: 10.1016/0965-1748(93)90071-y. View

17.

Hakala B, White C, Recklies A . Human cartilage gp-39, a major secretory product of articular chondrocytes and synovial cells, is a mammalian member of a chitinase protein family. J Biol Chem. 1993; 268(34):25803-10. View

18.

Andres A, Fletcher J, Karim F, Thummel C . Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysteroid-regulated transcription. Dev Biol. 1993; 160(2):388-404. DOI: 10.1006/dbio.1993.1315. View

19.

Jindra M, Sehnal F, Riddiford L . Isolation, characterization and developmental expression of the ecdysteroid-induced E75 gene of the wax moth Galleria mellonella. Eur J Biochem. 1994; 221(2):665-75. DOI: 10.1111/j.1432-1033.1994.tb18779.x. View

20.

Li F, Barnathan E, Kariko K . Rapid method for screening and cloning cDNAs generated in differential mRNA display: application of northern blot for affinity capturing of cDNAs. Nucleic Acids Res. 1994; 22(9):1764-5. PMC: 308062. DOI: 10.1093/nar/22.9.1764. View