The catalytic domain of xPAK1 is sufficient to induce myosin II dependent in vivo cell fragmentation independently of other apoptotic events

Developmental Biology

Volumn 263, Issue 2, 2003, Pages 264-281

  Bisson, Nicolas ^a   Islam, Nazrul ^a   Poitras, Luc ^a   Jean, Steve ^a   Bresnick, Anne ^b   Moss, Tom ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Cell fragmentation; JNK; Myosin II; Ste20; Xenopus; xPAK1

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BIOLOGICAL MARKER; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IMMUNOGLOBULIN LIGHT CHAIN; MYOSIN II; MYOSIN LIGHT CHAIN KINASE INHIBITOR; PROTEIN INHIBITOR; PROTEIN SUBUNIT; SERINE; THREONINE;

APOPTOSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION;

EID: 0242333966     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.07.002     Document Type: Article

References (64)

1. Bagrodia S., Dérijard B., Davis R.J., Cerione R.A. Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 270:1995;27995-27998.
2. Bhatia-Dey N., Adelstein R.S., Dawid I.B. Cloning of the cDNA encoding a myosin heavy chain B isoform of Xenopus nonmuscle myosin with an insert in the head region. Proc. Natl. Acad. Sci. USA. 90:1993;2856-2859.
3. Bokoch, G.M., 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem., in press.
4. Bresnick A.R., Wolff-Long V.L., Baumann O., Pollard T.D. Phosphorylation on threonine-18 of the regulatory light chain dissociates the ATPase and motor properties of smooth muscle myosin II. Biochemistry. 34:1995;12576-12583.
5. Brown J.L., Stowers L., Baer M., Trejo J., Coughlin S., Chant J. Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase pathway. Curr. Biol. 6:1996;598-605.
6. Cau J., Faure S., Comps M., Delsert C., Morin N. A novel p21-activated kinase binds the actin and microtubule networks and induces microtubule stabilization. J. Cell Biol. 155:2001;1029-1042.
7. Cau J., Faure S., Vigneron S., Labbé J.C., Delsert C., Morin N. Regulation of xenopus p21-activated kinase (X-PAK2) by Cdc42 and maturation-promoting factor controls Xenopus oocyte maturation. J. Biol. Chem. 275:2000;2367-2375.
8. Chen B.H., Tzen J.T., Bresnick A.R., Chen H.C. Roles of Rho-associated kinase and myosin light chain kinase in morphological and migratory defects of focal adhesion kinase-null cells. J. Biol. Chem. 8:2002;8.
9. Chen Y.R., Wang X.P., Templeton D., Davis R.J., Tan T.H. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation duration of JNK activation may determine cell death and proliferation . J. Biol. Chem. 271:1996;31929-31936.
10. Cramer L.P., Mitchison T.J. Myosin is involved in postmitotic cell spreading. J. Cell Biol. 131:1995;179-189.
11. Daniels R.H., Bokoch G.M. p21-activated protein kinase a crucial component of morphological signaling? Trends Biochem. Sci. 24:1999;350-355.
12. De Mazière A.M., Hage W.J., Ubbels G.A. A method for staining of cell nuclei in Xenopus laevis embryos with cyanine dyes for whole-mount confocal laser scanning microscopy. J. Histochem. Cytochem. 44:1996;399-402.
13. Dharmawardhane S., Sanders L.C., Martin S.S., Daniels R.H., Bokoch G.M. Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138:1997;1265-1278.
14. Drechsel D.N., Hyman A.A., Hall A., Glotzer M. A requirement for Rho and Cdc42 during cytokinesis in Xenopus embryos. Curr. Biol. 7:1997;12-23.
15. Faure S., Vigneron S., Dorée M., Morin N. A member of the Ste20/PAK family of protein kinases is involved in both arrest of Xenopus oocytes at G2/prophase of the first meiotic cell cycle and in prevention of apoptosis. EMBO J. 16:1997;5550-5561.
16. Frost J.A., Steen H., Shapiro P., Lewis T., Ahn N., Shaw P.E., Cobb M.H. Cross-cascade activation of ERKs and ternary complex factors by Rho family proteins. EMBO J. 16:1997;6426-6438.
17. Frost J.A., Xu S.C., Hutchison M.R., Marcus S., Cobb M.H. Actions of Rho family small G proteins and p21-activated protein kinases on mitogen-activated protein kinase family members. Mol. Cell. Biol. 16:1996;3707-3713.
18. Gnesutta N., Qu J., Minden A. The serine/threonine kinase PAK4 prevents caspase activation and protects cells from apoptosis. J. Biol. Chem. 276:2001;14414-14419.
19. Harden N., Lee J., Loh H.Y., Ong Y.M., Tan I., Leung T., Manser E., Lim L. A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell. Biol. 16:1996;1896-1908.
20. Howe J.A., Howell M., Hunt T., Newport J.W. Identification of a developmental timer regulating the stability of embryonic cyclin A and a new somatic A-type cyclin at gastrulation. Genes Dev. 9:1995;1164-1176.
21. Islam N., Poitras L., Moss T. The cytoskeletal effector xPAK1 is expressed during both car and lateral line development in Xenopus. Int. J. Dev. Biol. 44:2000;245-248.
22. Jaffer Z.M., Chernoff J. p21-activated kinases three more join the Pak . Int. J. Biochem. Cell Biol. 34:2002;713-717.
23. Jakobi R., Moertl E., Koeppel M.A. p21-activated protein kinase gamma-PAK suppresses programmed cell death of BALB3T3 fibroblasts. J. Biol. Chem. 276:2001;16624-16634.
24. Jeffs P., Jaques K., Osmond M. Cell death in cranial neural crest development. Anat. Embryol. 185:1992;583-588.
25. Kelley C.A., Oberman F., Yisraeli J.K., Adelstein R.S. A Xenopus nonmuscle myosin heavy chain isoform is phosphorylated by cyclin-p34cdc2 kinase during meiosis. J. Biol. Chem. 270:1995;1395-1401.
26. Kelley C.A., Sellers J.R., Gard G.L., Bui D., Adelstein R.S. Xenopus nonmuscle myosin heavy chain isoforms have different subcellular localizations and enzymatic activities. J. Cell Biol. 134:1996;675-687.
27. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis a basic biological phenomenon with wide-ranging implications in tissue kinetics . Br. J. Cancer. 26:1972;239-257.
28. Lee N., MacDonald H., Reinhard C., Halenbeck R., Roulston A., Shi T., Williams L.T. Activation of hPAK65 by caspase cleavage induces some of the morphological and biochemical changes of apoptosis. Proc. Natl. Acad. Sci. USA. 94:1997;13642-13647.
29. Leppä S., Bohmann D. Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene. 18:1999;6158-6162.
30. Liu Z.G., Hsu H.L., Goeddel D.V., Karin M. Dissection of TNF receptor 1 effector functions JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death . Cell. 87:1996;565-576.
31. Maciver S.K. Myosin II function in non-muscle cells. BioEssays. 18:1996;179-182.
32. Manser E., Huang H.Y., Loo T.H., Chen X.Q., Dong J.M., Leung T., Lim L. Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17:1997;1129-1143.
33. Martin S.J., Green D.R., Cotter T.G. Dicing with death dissecting the components of the apoptosis machinery . Trends Biochem. Sci. 19:1994;26-30.
34. Martin S.J., Reutelingsperger C.P., McGahon A.J., Rader J.A., van Schie R.C., LaFace D.M., Green D.R. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus inhibition by overexpression of Bcl-2 and Abl . J. Exp. Med. 182:1995;1545-1556.
35. Mills J.C., Stone N.L., Erhardt J., Pittman R.N. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J. Cell. Biol. 140:1998;627-636.
36. Mitchison T.J., Cramer L.P. Actin-based cell motility and cell locomotion. Cell. 84:1996;371-379.
37. Nebreda A.R., Gannon J.V., Hunt T. Newly synthesized protein(s) must associate with p34cdc2 to activate MAP kinase and MPF during progesterone-induced maturation of Xenopus oocytes. EMBO J. 14:1995;5597-5607.
38. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin) A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis . 1967;North-Holland Publishing Company, Amsterdam.
39. Obermeier A., Ahmed S., Manser E., Yen S.C., Hall C., Lim L. PAK promotes morphological changes by acting upstream of Rac. EMBO J. 17:1998;4328-4339.
40. Ostap E.M. 2,3-Butanedione monoxime (BDM) as a myosin inhibitor. J. Muscle Res. Cell Motil. 23:2002;305-308.
41. Peng C.Y., Manning L., Albertson R., Doe C.Q. The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature. 408:2000;596-600.
42. Peter M.E., Heufelder A.E., Hengartner M.O. Advances in apoptosis research. Proc. Natl. Acad. Sci. USA. 94:1997;12736-12737.
43. Poitras L., Jean S., Islam N., Moss T. PAK interacts with NCK and MLK2 to regulate the activation of jun N-terminal kinase. FEBS Lett. 543:2003;129-135.
44. Ramos E., Wysolmerski R.B., Masaracchia R.A. Myosin phosphorylation by human cdc42-dependent S6/H4 kinase/gammaPAK from placenta and lymphoid cells. Recept. Signal. Transduct. 7:1997;99-110.
45. Rooney R.D., Tuazon P.T., Meek W.E., Carroll E.J. Jr., Hagen J.J., Gump E.L., Monnig C.A., Lugo T., Traugh J.A. Cleavage arrest of early frog embryos by the G protein-activated protein kinase PAK I. J. Biol. Chem. 271:1996;21498-21504.
46. Rudel T., Bokoch G.M. Membrane and morphological changes in apoptotic cells regulated by Caspase-mediated activation of PAK2. Science. 276:1997;1571-1574.
47. Schürmann A., Mooney A.F., Sanders L.C., Sells M.A., Wang H.G., Reed J.C., Bokoch G.M. p21-activated kinase 1 phosphorylates the death agonist Bad and protects cells from apoptosis. Mol. Cell. Biol. 20:2000;453-461.
48. Sells M.A., Knaus U.G., Bagrodia S., Ambrose D.M., Bokoch G.M., Chernoff J. Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7:1997;202-210.
49. Sible J.C., Anderson J.A., Lewellyn A.L., Maller J.L. Zygotic transcription is required to block a maternal program of apoptosis in Xenopus embryos. Dev. Biol. 189:1997;335-346.
50. Siow Y.L., Kalmar G.B., Sanghera J.S., Tai G., Oh S.S., Pelech S.L. Identification of two essential phosphorylated threonine residues in the catalytic domain of Mekk1 indirect activation by Pak3 and protein kinase C . J. Biol. Chem. 272:1997;7586-7594.
51. Smith D.B., Corcoran L.M. Protein expression. Ausubel E.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Seidman J.G., Smith J.A., Struhl K. Current Protocols in Molecular Biology. 1991;Greene Publishing Associates & Wiley-Interscience, New York.
52. Song Z.W., Steller H. Death by design mechanism and control of apoptosis . Trends Biochem. Sci. 24:1999;M49-M52.
53. Souopgui J., Solter M., Pieler T. XPak3 promotes cell cycle withdrawal during primary neurogenesis in Xenopus laevis. EMBO J. 21:2002;6429-6439.
54. Stack J.H., Newport J.W. Developmentally regulated activation of apoptosis early in Xenopus gastrulation results in cyclin A degradation during interphase of the cell cycle. Development. 124:1997;3185-3195.
55. Stefanovsky V.Y., Pelletier G., Hannan R., Gagnon-Kugler T., Rothblum L.I., Moss T. An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol. Cell. 8:2001;1063-1073.
56. Teramoto H., Coso O.A., Miyata H., Igishi T., Miki T., Gutkind J.S. Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase stress-activated protein kinase pathway a role for mixed lineage kinase 3 protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family . J. Biol. Chem. 271:1996;27225-27228.
57. Titus M.A. Caveat experimentor - is your myosin really inhibited? Nat. Cell Biol. 5:2003;95.
58. Tuazon P.T., Traugh J.A. Activation of actin-activated ATPase in smooth muscle by phosphorylation of myosin light chain with protease-activated kinase I. J. Biol. Chem. 259:1984;541-546.
59. Vadlamudi R.K., Li F., Adam L., Nguyen D., Ohta Y., Stossel T.P., Kumar R. Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase I. Nat. Cell Biol. 4:2002;681-690.
60. Vernes I., Haanen C., Steffens-Nakken H., Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods. 184:1995;39-51.
61. Westwick J.K., Lambert Q.T., Clark G.J., Symons M., Van Aelst L., Pestell R.G., Der C.J. Rac regulation of transformation, gene expression, and actin organization by multiple, PAK-independent pathways. Mol. Cell Biol. 17:1997;1324-1335.
62. Wilson I.A., Niman H.L., Houghten R.A., Cherenson A.R., Connolly M.L., Lerner R.A. The structure of an antigenic determinant in a protein. Cell. 37:1984;767-778.
63. Zhang S.J., Han J.H., Sells M.A., Chernoff J., Knaus U.G., Ulevitch R.J., Bokoch G.M. Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. J. Biol. Chem. 270:1995;23934-23936.
64. Zhao Z.S., Manser E., Chen X.Q., Chong C., Leung T., Lim L. A conserved negative regulatory region in alphaPAK inhibition of PAK kinases reveals their morphological roles downstream of Cdc42 and Rac1 . Mol. Cell. Biol. 18:1998;2153-2163.