Role of PI 3-kinase and PIP3 in submandibular gland branching morphogenesis

Developmental Biology

Volumn 255, Issue 1, 2003, Pages 178-191

  Larsen, Melinda ^a   Hoffman, Matthew P ^a   Sakai, Takayoshi ^a   Neibaur, Justin C ^a,b   Mitchell, Jonathan M ^a,c   Yamada, Kenneth M ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Akt; Branching morphogenesis; Inhibitors; Mouse; Organ culture; Phosphatidylinositol 3,4,5 trisphosphate; Phosphatidylinositol 3 kinase; Salivary gland; Submandibular gland; Time lapse microscopy

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EPITHELIUM; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MESENCHYME; MICROSCOPY; MOUSE; NONHUMAN; ORGAN CULTURE; PHOSPHORYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SUBMANDIBULAR GLAND; WESTERN BLOTTING;

EID: 0037333510     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(02)00047-7     Document Type: Article

References (44)

1. Bernfield M.R., Wessells N.K. Intra- and extracellular control of epithelial morphogenesis. Symp. Soc. Dev. Biol. 29:1970;195-249.
2. Bridges A.J., Zhou H., Cody D.R., Rewcastle G.W., McMichael A., Showalter H.D., Fry D.W., Kraker A.J., Denny W.A. Tyrosine kinase inhibitors. 8. An unusually steep structure-activity relationship for analogues of 4-(3-bromoanilino)-6,7-dimethoxyquinazoline (PD 153035), a potent inhibitor of the epidermal growth factor receptor. J. Med. Chem. 39:1996;267-276.
3. Brunn G.J., Williams J., Sabers C., Wiederrecht G., Lawrence J.C. Jr., Abraham R.T. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15:1996;5256-5267.
4. Carballada R., Yasuo H., Lemaire P. Phosphatidylinositol-3 kinase acts in parallel to the ERK MAP kinase in the FGF pathway during Xenopus mesoderm induction. Development. 128:2001;35-44.
5. Czech M.P. PIP2 and PIP3 complex roles at the cell surface . Cell. 100:2000;603-606.
6. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:2000;95-105.
7. De Moerlooze L., Spencer-Dene B., Revest J., Hajihosseini M., Rosewell I., Dickson C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development. 127:2000;483-492.
8. Fruman D.A., Meyers R.E., Cantley L.C. Phosphoinositide kinases. Annu. Rev. Biochem. 67:1998;481-507.
9. Gilbert S.F. Developmental Biology. 2000;Sinauer Associates, Inc, Sunderland, MA.
10. Grobstein C., Cohen J. Collagenase effect on the morphogenesis of embryonic salivary epithelium in vitro . Science. 150:1965;626-628.
11. Hartley K.O., Gell D., Smith G.C., Zhang H., Divecha N., Connelly M.A., Admon A., Lees-Miller S.P., Anderson C.W., Jackson S.P. DNA-dependent protein kinase catalytic subunit a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product . Cell. 82:1995;849-856.
12. Hawkins P.T., Eguinoa A., Qiu R.G., Stokoe D., Cooke F.T., Walters R., Wennstrom S., Claesson-Welsh L., Evans T., Symons M., et al. PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Curr. Biol. 5:1995;393-403.
13. Hernandez R., Teruel T., Lorenzo M. Akt mediates insulin induction of glucose uptake and up-regulation of GLUT4 gene expression in brown adipocytes. FEBS Lett. 494:2001;225-231.
14. Hieda Y., Nakanishi Y. Epithelial morphogenesis in mouse embryonic submandibular gland its relationships to the tissue organization of epithelium and mesenchyme . Dev. Growth Differ. 39:1997;1-8.
15. Hoffman M.P., Kidder B., Steinberg Z., Lakhani S., Ho S., Kleinman H.K., Larsen M. Gene expression profiles of mouse submandibular gland development: FGFR1 regulates branching morphogenesis in vitro through BMP- and FGF-dependant mechanisms. Development. 129:2002;5767-5778.
16. Jaskoll T., Melnick M. Submandibular gland morphogenesis stage-specific expression of TGF-alpha/EGF, IGF, TGF-beta, TNF, and IL-6 signal transduction in normal embryonic mice and the phenotypic effects of TGF-beta2, TGF-beta3, and EGF-r null mutations . Anat. Rec. 256:1999;252-268.
17. Jaskoll T., Zhou Y.M., Chai Y., Makarenkova H.P., Collinson J.M., West J.D., Hajihosseini M.K., Lee J., Melnick M. Embryonic submandibular gland morphogenesis stage-specific protein localization of FGFs, BMPs, Pax6 and Pax9 in normal mice and abnormal SMG phenotypes in FgfR2-IIIc(+/Delta), BMP7(-/-) and Pax6(-/-) Mice . Cells Tissues Organs. 170:2002;83-98.
18. Kadoya Y., Kadoya K., Durbeej M., Holmvall K., Sorokin L., Ekblom P. Antibodies against domain E3 of laminin-1 and integrin alpha 6 subunit perturb branching epithelial morphogenesis of submandibular gland, but by different modes. J. Cell Biol. 129:1995;521-534.
19. Kadoya Y., Yamashina S. Distribution of alpha 6 integrin subunit in developing mouse submandibular gland. J. Histochem. Cytochem. 41:1993;1707-1714.
20. Kashimata M., Gresik E.W. Epidermal growth factor system is a physiological regulator of development of the mouse fetal submandibular gland and regulates expression of the alpha6-integrin subunit. Dev. Dyn. 208:1997;149-161.
21. Kashimata M., Sayeed S., Ka A., Onetti-Muda A., Sakagami H., Faraggiana T., Gresik E.W. The ERK-1/2 signaling pathway is involved in the stimulation of branching morphogenesis of fetal mouse submandibular glands by EGF. Dev. Biol. 220:2000;183-196.
22. Melnick M., Chen H., Min Zhou Y., Jaskoll T. The functional genomic response of developing embryonic submandibular glands to NF-kappaB inhibition. BMC Dev. Biol. 1:2001;15.
23. Meyers R., Cantley L.C. Cloning and characterization of a wortmannin-sensitive human phosphatidylinositol 4-kinase. J. Biol. Chem. 272:1997;4384-4390.
24. Miyazaki M. Branching morphogenesis in the embryonic mouse submandibular gland a scanning electron microscopic study . Arch. Histol. Cytol. 53:1990;157-165.
25. Morita K., Nogawa H. EGF-dependent lobule formation and FGF7-dependent stalk elongation in branching morphogenesis of mouse salivary epithelium in vitro. Dev. Dyn. 215:1999;148-154.
26. Nakanishi H., Brewer K.A., Exton J.H. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268:1993;13-16.
27. Nakanishi Y., Morita T., Nogawa H. Cell proliferation is not required for the initiation of early cleft formation in mouse embryonic submandibular epithelium in vitro. Development. 99:1987;429-437.
28. Nowak F., Jacquemin-Sablon A., Pierre J. Epidermal growth factor receptor signaling cascade as target for tyrphostin (RG 50864) in epithelial cells. Paradoxical effects on mitogen-activated protein kinase kinase and mitogen-activated protein kinase activities. Biochem. Pharmacol. 53:1997;287-298.
29. Ohuchi H., Hori Y., Yamasaki M., Harada H., Sekine K., Kato S., Itoh N. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem. Biophys. Res. Commun. 277:2000;643-649.
30. Okano J., Gaslightwala I., Birnbaum M.J., Rustgi A.K., Nakagawa H. Akt/Protein kinase B isoforms are differentially regulated by epidermal growth factor stimulation. J. Biol. Chem. 275:2000;30934-30942.
31. Partanen A.M., Thesleff I. Localization and quantitation of 125I-epidermal growth factor binding in mouse embryonic tooth and other embryonic tissues at different developmental stages. Dev. Biol. 120:1987;186-197.
32. Pinna L.A. Protein kinase CK2 a challenge to canons . J. Cell Sci. 115:2002;3823-3878.
33. Royce L.S., Kibbey M.C., Mertz P., Kleinman H.K., Baum B.J. Human neoplastic submandibular intercalated duct cells express an acinar phenotype when cultured on a basement membrane matrix. Differentiation. 52:1993;247-255.
34. Scheid M.P., Woodgett J.R. PKB/AKT functional insights from genetic models . Nat. Rev. Mol. Cell Biol. 2:2001;760-768.
35. Sekine K., Ohuchi H., Fujiwara M., Yamasaki M., Yoshizawa T., Sato T., Yagishita N., Matsui D., Koga Y., Itoh N., Kato S. Fgf10 is essential for limb and lung formation. Nat. Genet. 21:1999;138-141.
36. Soltoff S.P., Carraway K.L. 3rd, Prigent S.A., Gullick W.G., Cantley L.C. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 14:1994;3550-3558.
37. Spooner B.S., Bassett K.E., Spooner B.S. Jr. Embryonic salivary gland epithelial branching activity is experimentally independent of epithelial expansion activity. Dev. Biol. 133:1989;569-575.
38. Spooner B.S., Wessells N.K. An analysis of salivary gland morphogenesis role of cytoplasmic microfilaments and microtubules . Dev. Biol. 27:1972;38-54.
39. Stephens L., Anderson K., Stokoe D., Erdjument-Bromage H., Painter G.F., Holmes A.B., Gaffney P.R., Reese C.B., McCormick F., Tempst P., Coadwell J., Hawkins P.T. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science. 279:1998;710-714.
40. Takahashi Y., Nogawa H. Branching morphogenesis of mouse salivary epithelium in basement membrane-like substratum separated from mesenchyme by the membrane filter. Development. 111:1991;327-335.
41. Tang M.J., Cai Y., Tsai S.J., Wang Y.K., Dressler G.R. Ureteric bud outgrowth in response to RET activation is mediated by phosphatidylinositol 3-kinase. Dev. Biol. 243:2002;128-136.
42. Toker A. Protein kinases as mediators of phosphoinositide 3-kinase signaling. Mol. Pharmacol. 57:2000;652-658.
43. Toker A., Meyer M., Reddy K.K., Falck J.R., Aneja R., Aneja S., Parra A., Burns D.J., Ballas L.M., Cantley L.C. Activation of protein kinase C family members by the novel polyphosphoinositides PtdIns-3,4-P2 and PtdIns-3,4,5-P3. J. Biol. Chem. 269:1994;32358-32367.
44. Yarden Y., Sliwkowski M.X. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2:2001;127-137.