Puckered Encodes a Phosphatase That Mediates a Feedback Loop Regulating JNK Activity During Dorsal Closure in Drosophila

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 1998 Mar 21

PMID 9472024

Citations 332

Authors

A Gampel

J Ring

K Virdee

N Kirov

A M Tolkovsky

A Martinez-Arias

Affiliations

Soon will be listed here.

Abstract

The activation of MAPKs is controlled by the balance between MAPK kinase and MAPK phosphatase activities. The latter is mediated by a subset of phosphatases with dual specificity (VH-1 family). Here, we describe a new member of this family encoded by the puckered gene of Drosophila. Mutations in this gene lead to cytoskeletal defects that result in a failure in dorsal closure related to those associated with mutations in basket, the Drosophila JNK homolog. We show that puckered mutations result in the hyperactivation of DJNK, and that overexpression of puc mimics basket mutant phenotypes. We also show that puckered expression is itself a consequence of the activity of the JNK pathway and that during dorsal closure, JNK signaling has a dual role: to activate an effector, encoded by decapentaplegic, and an element of negative feedback regulation encoded by puckered.

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References

Kwak S, Dixon J . Multiple dual specificity protein tyrosine phosphatases are expressed and regulated differentially in liver cell lines. J Biol Chem. 1995; 270(3):1156-60. DOI: 10.1074/jbc.270.3.1156. View

Kameshita I, Fujisawa H . A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel. Anal Biochem. 1989; 183(1):139-43. DOI: 10.1016/0003-2697(89)90181-4. View

Diaz-Benjumea F, Hafen E . The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development. Development. 1994; 120(3):569-78. DOI: 10.1242/dev.120.3.569. View

Keyse S, Emslie E . Oxidative stress and heat shock induce a human gene encoding a protein-tyrosine phosphatase. Nature. 1992; 359(6396):644-7. DOI: 10.1038/359644a0. View

Glise B, Bourbon H, Noselli S . hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell. 1995; 83(3):451-61. DOI: 10.1016/0092-8674(95)90123-x. View

Ring J, Arias A . puckered, a gene involved in position-specific cell differentiation in the dorsal epidermis of the Drosophila larva. Dev Suppl. 1993; :251-9. View

Groom L, Sneddon A, Alessi D, Dowd S, Keyse S . Differential regulation of the MAP, SAP and RK/p38 kinases by Pyst1, a novel cytosolic dual-specificity phosphatase. EMBO J. 1996; 15(14):3621-32. PMC: 451978. View

Brown N, Kafatos F . Functional cDNA libraries from Drosophila embryos. J Mol Biol. 1988; 203(2):425-37. DOI: 10.1016/0022-2836(88)90010-1. View

Ishibashi T, Bottaro D, Michieli P, KELLEY C, Aaronson S . A novel dual specificity phosphatase induced by serum stimulation and heat shock. J Biol Chem. 1994; 269(47):29897-902. View

10.

Smith D, Johnson K . Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988; 67(1):31-40. DOI: 10.1016/0378-1119(88)90005-4. View

11.

Affolter M, Nellen D, Nussbaumer U, Basler K . Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis. Development. 1994; 120(11):3105-17. DOI: 10.1242/dev.120.11.3105. View

12.

St Johnston R, Hoffmann F, Blackman R, Segal D, Grimaila R, PADGETT R . Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 1990; 4(7):1114-27. DOI: 10.1101/gad.4.7.1114. View

13.

Riesgo-Escovar J, JENNI M, Fritz A, Hafen E . The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev. 1996; 10(21):2759-68. DOI: 10.1101/gad.10.21.2759. View

14.

Tournier C, Whitmarsh A, Cavanagh J, Barrett T, Davis R . Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proc Natl Acad Sci U S A. 1997; 94(14):7337-42. PMC: 23822. DOI: 10.1073/pnas.94.14.7337. View

15.

Young P, Richman A, KETCHUM A, Kiehart D . Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 1993; 7(1):29-41. DOI: 10.1101/gad.7.1.29. View

16.

Wilson R, Ainscough R, Anderson K, Baynes C, Berks M, Bonfield J . 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994; 368(6466):32-8. DOI: 10.1038/368032a0. View

17.

Wharton K, Ray R, Gelbart W . An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development. 1993; 117(2):807-22. DOI: 10.1242/dev.117.2.807. View

18.

Nusslein-Volhard C, Wieschaus E, Kluding H . Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster : I. Zygotic loci on the second chromosome. Wilehm Roux Arch Dev Biol. 2017; 193(5):267-282. DOI: 10.1007/BF00848156. View

19.

Holland P, Suzanne M, Campbell J, Noselli S, Cooper J . MKK7 is a stress-activated mitogen-activated protein kinase kinase functionally related to hemipterous. J Biol Chem. 1997; 272(40):24994-8. DOI: 10.1074/jbc.272.40.24994. View

20.

Claassen L, Ahn B, Koo H, Grossman L . Construction of deletion mutants of the Escherichia coli UvrA protein and their purification from inclusion bodies. J Biol Chem. 1991; 266(17):11380-7. View