Impaired development of the Harderian gland in mutant protein phosphatase 2A transgenic mice

Mechanisms of Development

Volumn 123, Issue 5, 2006, Pages 362-371

  Schild, Andreas ^a   Isenmann, Stefan ^b   Tanimoto, Naoyuki ^c   Tonagel, Felix ^c   Seeliger, Mathias W ^c   Ittner, Lars M ^d,f   Kretz, Alexandra ^b   Ogris, Egon ^e   Götz, Jürgen ^a,f  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d ORTHOPEDIC UNIVERSITY HOSPITAL BALGRIST   (Switzerland)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cadherin; Cell adhesion; Development; Enophthalmos; Ganzfeld electroretinography (ERG); Harderian gland; Protein phosphatase 2A (PP2A); Scanning laser ophthalmoscopy; Transgenic mice

Indexed keywords

BETA CATENIN; CADHERIN; GLYCOGEN SYNTHASE KINASE 3BETA; MUTANT PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN SUBUNIT;

ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONTROLLED STUDY; CYTOSOL; DEVELOPMENTAL DISORDER; ENOPHTHALMOS; ENZYME ACTIVE SITE; ENZYME ASSAY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; EYE DEVELOPMENT; GENE EXPRESSION REGULATION; HARDER GLAND; HYPOPLASIA; MOUSE; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CATALYTIC DOMAIN; CELL ADHESION; DIMERIZATION; EYE ABNORMALITIES; GENE EXPRESSION REGULATION; HARDERIAN GLAND; LEUCINE; MICE; MICE, TRANSGENIC; MUTATION; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN SUBUNITS;

MUS MUSCULUS; RODENTIA;

EID: 33744928623     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2006.03.003     Document Type: Article

References (59)

1. Arufe M.C., Beckett G.J., Duran R., and Alfonso M. Effect of okadaic acid and calyculin-A, two protein phosphatase inhibitors, on thyrotropin-stimulated triiodothyronine secretion in cultured sheep thyroid cells. Endocrine 11 (1999) 235-240
2. Baharians Z., and Schonthal A.H. Autoregulation of protein phosphatase type 2A expression. J. Biol. Chem. 273 (1998) 19019-19024
3. Bryant J.C., Westphal R.S., and Wadzinski B.E. Methylated C-terminal leucine residue of PP2A catalytic subunit is important for binding of regulatory Balpha subunit. Biochem. J. 339 Pt 2 (1999) 241-246
4. Buzzell G.R. The Harderian gland: perspectives. Microsc. Res. Tech. 34 (1996) 2-5
5. Campsall K.D., Mazerolle C.J., De Repentingy Y., Kothary R., and Wallace V.A. Characterization of transgene expression and cre recombinase activity in a panel of Thy-1 promoter-cre transgenic mice. Dev. Dyn. 224 (2002) 135-143
6. Chen, F., David, D., Ferrari, A., Gotz, J., 2004. Posttranslational modifications of tau-role in human tauopathies and modeling in transgenic animals. Curr. Drug Targets 5, 503-315.
7. Coto-Montes A., Rodriguez-Colunga M.J., Tolivia D., and Sanchez-Barcelo E. Histopathological features of the Harderian glands in transgenic mice carrying MMTV/N-ras protooncogene. Microsc. Res. Tech. 38 (1997) 311-314
8. Evans D.R., and Hemmings B.A. Mutation of the C-terminal leucine residue of PP2Ac inhibits PR55/B subunit binding and confers supersensitivity to microtubule destabilization in Saccharomyces cerevisiae. Mol. Gen. Genet. 264 (2000) 425-432
9. Evans D.R., Myles T., Hofsteenge J., and Hemmings B.A. Functional expression of human PP2Ac in yeast permits the identification of novel C-terminal and dominant-negative mutant forms. J. Biol. Chem. 274 (1999) 24038-24046
10. Everett A.D., Kamibayashi C., and Brautigan D.L. Transgenic expression of protein phosphatase 2A regulatory subunit B56gamma disrupts distal lung differentiation. Am. J. Physiol. Lung Cell. Mol. Physiol. 282 (2002) L1266-L1271
11. Favre B., Turowski P., and Hemmings B.A. Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem. 272 (1997) 13856-13863
12. Gao S., Eiberg H., Krogdahl A., Liu C.J., and Sorensen J.A. Cytoplasmic expression of E-cadherin and beta-Catenin correlated with LOH and hypermethylation of the APC gene in oral squamous cell carcinomas. J. Oral Pathol. Med. 34 (2005) 116-119
13. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119 (1992) 493-501
14. Gotz J., and Schild A. Transgenic and knockout models of PP2A. Methods Enzymol. 366 (2003) 390-403
15. Gotz J., Probst A., Spillantini M.G., Schafer T., Jakes R., Burki K., and Goedert M. Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. Eur. Mol. Biol. Org. 14 (1995) 1304-1313
16. Gotz J., Probst A., Ehler E., Hemmings B., and Kues W. Delayed embryonic lethality in mice lacking protein phosphatase 2A catalytic subunit Calpha. Proc. Natl Acad. Sci. USA 95 (1998) 12370-12375
17. Gotz J., Probst A., Mistl C., Nitsch R.M., and Ehler E. Distinct role of protein phosphatase 2A subunit calpha in the regulation of E-cadherin and beta-catenin during development. Mech. Dev. 93 (2000) 83-93
18. Gotz J., Chen F., Barmettler R., and Nitsch R.M. Tau filament formation in transgenic mice expressing P301L tau. J. Biol. Chem. 276 (2001) 529-534
19. Govindarajan V., Ito M., Makarenkova H.P., Lang R.A., and Overbeek P.A. Endogenous and ectopic gland induction by FGF-10. Dev. Biol. 225 (2000) 188-200
20. Gray Jr. L.E., Kavlock R.J., Chernoff N., Ferrell J., McLamb J., and Ostby J. Prenatal exposure to the herbicide 2,4-dichlorophenyl-p-nitrophenyl ether destroys the rodent Harderian gland. Science 215 (1982) 293-294
21. Groves M.R., Hanlon N., Turowski P., Hemmings B.A., and Barford D. The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96 (1999) 99-110
22. Haegel H., Larue L., Ohsugi M., Fedorov L., Herrenknecht K., and Kemler R. Lack of beta-catenin affects mouse development at gastrulation. Development 121 (1995) 3529-3537
23. Janssens V., and Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 353 (2001) 417-439
24. Jhappan C., Gallahan D., Stahle C., Chu E., Smith G.H., Merlino G., and Callahan R. Expression of an activated Notch-related int-3 transgene interferes with cell differentiation and induces neoplastic transformation in mammary and salivary glands. Genes Dev. 6 (1992) 345-355
25. Kamibayashi C., Lickteig R.L., Estes R., Walter G., and Mumby M.C. Expression of the A subunit of protein phosphatase 2A and characterization of its interactions with the catalytic and regulatory subunits. J. Biol. Chem. 267 (1992) 21864-21872
26. Kins S., Crameri A., Evans D.R., Hemmings B.A., Nitsch R.M., and Gotz J. Reduced PP2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J. Biol. Chem. 276 (2001) 38193-38200
27. Kins S., Kurosinski P., Nitsch R.M., and Gotz J. Activation of the ERK and JNK signaling pathways caused by neuron specific inhibition of PP2A in transgenic mice. Am. J. Pathol. 163 (2003) 833-843
28. Kollias G., Spanopoulou E., Grosveld F., Ritter M., Beech J., and Morris R. Differential regulation of a Thy-1 gene in transgenic mice. Proc. Natl Acad. Sci. USA 84 (1987) 1492-1496
29. Larue L., Ohsugi M., Hirchenhain J., and Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl Acad. Sci. USA 91 (1994) 8263-8267
30. Lau K.F., Miller C.C., Anderton B.H., and Shaw P.C. Molecular cloning and characterization of the human glycogen synthase kinase-3beta promoter. Genomics 60 (1999) 121-128
31. Lazzereschi D., Coppa A., Minicione G., Lavitrano M., Fragomele F., and Colletta G. The phosphatase inhibitor okadaic acid stimulates the TSH-induced G1-S phase transition in thyroid cells. Exp. Cell Res. 234 (1997) 425-433
32. Lee H.Y., Kleber M., Hari L., Brault V., Suter U., Taketo M.M., et al. Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 303 (2004) 1020-1023
33. Li X., Scuderi A., Letsou A., and Virshup D.M. B56-associated protein phosphatase 2A is required for survival and protects from apoptosis in Drosophila melanogaster. Mol. Cell Biol. 22 (2002) 3674-3684
34. Lickert H., Bauer A., Kemler R., and Stappert J. Casein kinase II phosphorylation of E-cadherin increases E-cadherin/beta-catenin interaction and strengthens cell-cell adhesion. J. Biol. Chem. 275 (2000) 5090-5095
35. Luthi A., Putten H., Botteri F.M., Mansuy I.M., Meins M., Frey U., et al. Endogenous serine protease inhibitor modulates epileptic activity and hippocampal long-term potentiation. J. Neurosci. 17 (1997) 4688-4699
36. Martens E., Stevens S., Janssens J., Gotz J., Goris J., and van Hoof C. Genomic organisation, chromosomal localisation, tissue distribution and developmental regulation of the PR61/B' regulatory subunits of protein phosphatase 2A in mice. J. Mol. Biol. 336 (2004) 971-986
37. McClellan K.A., Robertson F.G., Kindblom J., Wennbo H., Tornell J., Bouchard B., et al. Investigation of the role of prolactin in the development and function of the lacrimal and harderian glands using genetically modified mice. Invest. Ophthalmol. Vis. Sci. 42 (2001) 23-30
38. McCright B., Rivers A.M., Audlin S., and Virshup D.M. The B56 family of protein phosphatase 2A (PP2A) regulatory subunits encodes differentiation-induced phosphoproteins that target PP2A to both nucleus and cytoplasm. J. Biol. Chem. 271 (1996) 22081-22089
39. Moreno C.S., Park S., Nelson K., Ashby D., Hubalek F., Lane W.S., and Pallas D.C. WD40 repeat proteins striatin and S/G(2) nuclear autoantigen are members of a novel family of calmodulin-binding proteins that associate with protein phosphatase 2A. J. Biol. Chem. 275 (2000) 5257-5263
40. Ogris E., Gibson D.M., and Pallas D.C. Protein phosphatase 2A subunit assembly: the catalytic subunit carboxy terminus is important for binding cellular B subunit but not polyomavirus middle tumor antigen. Oncogene 15 (1997) 911-917
41. Ogris E., Mudrak I., Mak E., Gibson D., and Pallas D.C. Catalytically inactive protein phosphatase 2A can bind to polyomavirus middle tumor antigen and support complex formation with pp60(c-src). J. Virol. 73 (1999) 7390-7398
42. Okubo T., and Hogan B.L. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol. 3 (2004) 11
43. Payne A.P. The harderian gland: a tercentennial review. J. Anat. 185 Pt 1 (1994) 1-49
44. Schild, A., Ittner, L.M., Götz, J., in press. Altered phosphorylation of cytoskeletal proteins in mutant protein phosphatase 2A transgenic mice, Biochem. Biophys. Res. Commun., in press.
45. Schmidt K., Kins S., Schild A., Nitsch R.M., Hemmings B.A., and Gotz J. Diversity, developmental regulation and distribution of murine PR55/B subunits of protein phosphatase 2A. Eur. J. Neurosci. 16 (2002) 2039-2048
46. Seeliger M.W., Grimm C., Stahlberg F., Friedburg C., Jaissle G., Zrenner E., et al. New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat. Genet. 29 (2001) 70-74
47. Serres M., Grangeasse C., Haftek M., Durocher Y., Duclos B., Schmitt D., et al. Hyperphosphorylation of beta-catenin on serine-threonine residues and loss of cell-cell contacts induced by calyculin A and okadaic acid in human epidermal cells. Exp. Cell Res. 231 (1997) 163-172
48. Serres M., Filhol O., Lickert H., Grangeasse C., Chambaz E.M., Stappert J., et al. The disruption of adherens junctions is associated with a decrease of E-cadherin phosphorylation by protein kinase CK2. Exp. Cell Res. 257 (2000) 255-264
49. Silverstein A.M., Barrow C.A., Davis A.J., and Mumby M.C. Actions of PP2A on the MAP kinase pathway and apoptosis are mediated by distinct regulatory subunits. Proc. Natl Acad. Sci. USA 99 (2002) 4221-4226
50. Sinn E., Muller W., Pattengale P., Tepler I., Wallace R., and Leder P. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 49 (1987) 465-475
51. Strack S., Zaucha J.A., Ebner F.F., Colbran R.J., and Wadzinski B.E. Brain protein phosphatase 2A: developmental regulation and distinct cellular and subcellular localization by B subunits. J. Comp. Neurol. 392 (1998) 515-527
52. Tehrani M.A., Mumby M.C., and Kamibayashi C. Identification of a novel protein phosphatase 2A regulatory subunit highly expressed in muscle. J. Biol. Chem. 271 (1996) 5164-5170
53. Tolstykh T., Lee J., Vafai S., and Stock J.B. Carboxyl methylation regulates phosphoprotein phosphatase 2A by controlling the association of regulatory B subunits. Eur. Mol. Biol. Org. 19 (2000) 5682-5691
54. Turowski P., Fernandez A., Favre B., Lamb N.J., and Hemmings B.A. Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression. J. Cell Biol. 129 (1995) 397-410
55. Wera S., Fernandez A., Lamb N.J., Turowski P., Hemmings-Mieszczak M., Mayer-Jaekel R.E., and Hemmings B.A. Deregulation of translational control of the 65-kDa regulatory subunit (PR65 alpha) of protein phosphatase 2A leads to multinucleated cells. J. Biol. Chem. 270 (1995) 21374-21381
56. White V., Sinn E., and Albert D.M. Harderian gland pathology in transgenic mice carrying the MMTV/v-Ha-ras gene. Invest. Ophthalmol. Vis. Sci. 31 (1990) 577-581
57. Wu J., Tolstykh T., Lee J., Boyd K., Stock J.B., and Broach J.R. Carboxyl methylation of the phosphoprotein phosphatase 2A catalytic subunit promotes its functional association with regulatory subunits in vivo. Embo. J. 19 (2000) 5672-5681
58. Wurdak H., Ittner L.M., Lang K.S., Leveen P., Suter U., Fischer J.A., et al. Inactivation of TGFbeta signaling in neural crest stem cells leads to multiple defects reminiscent of DiGeorge syndrome. Genes. Dev. 19 (2005) 530-535
59. Yu X.X., Du X., Moreno C.S., Green R.E., Ogris E., Feng Q., et al. Methylation of the protein phosphatase 2a catalytic subunit is essential for association of balpha regulatory subunit but not SG2NA, striatin, or polyomavirus middle tumor antigen. Mol. Biol. Cell 12 (2001) 185-199