Keratinocytes from APP/APLP2-deficient mice are impaired in proliferation, adhesion and migration in vitro

Experimental Cell Research

Volumn 312, Issue 11, 2006, Pages 1939-1949

  Siemes, Christina ^a   Quast, Thomas ^a   Kummer, Christiane ^a   Wehner, Sven ^a   Kirfel, Gregor ^a   Müller, Ulrike ^b   Herzog, Volker ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA AMYLOID PRECURSOR LIKE PROTEIN 2; PROTEIN; UNCLASSIFIED DRUG; APLP2 PROTEIN, MOUSE; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; BASAL CELL; CELL ADHESION; CELL CULTURE; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EPIDERMIS; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SKIN CELL; VELOCITY; ANIMAL; CELL MOTION; CYTOLOGY; DRUG EFFECT; GENETICS; MICROSCOPY; MOUSE MUTANT; PHYSIOLOGY;

MAMMALIA;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; KERATINOCYTES; MICE; MICE, KNOCKOUT; MICROSCOPY, VIDEO; RECOMBINANT PROTEINS;

EID: 33746674498     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.02.025     Document Type: Article

References (51)

1. Holbrook K.A. Ultrastructure of epidermis. The Keratinocytes Handbook (1994), Cambridge University
2. Jones J.C., Goldman A.E., Yang H.Y., and Goldman R.D. The organizational fate of intermediate filament networks in two epithelial cell types during mitosis. J. Cell Biol. 100 (1985) 93-102
3. Kalinin A.E., Kajava A.V., and Steinert P.M. Epithelial barrier function: assembly and structural features of the cornified cell envelope. BioEssays 24 (2002) 789-800
4. Cowin P., and Burke B. Cytoskeleton-membrane interactions. Curr. Opin. Cell Biol. 8 (1996) 56-65
5. Braga V.M. Cell-cell adhesion and signalling. Curr. Opin. Cell Biol. 14 (2002) 546-556
6. Jamora C., and Fuchs E. Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 4 (2002) E101-E108
7. Fuchs E., and Raghavan S. Getting under the skin of epidermal morphogenesis. Nat. Rev., Genet. 3 (2002) 199-209
8. Nanney L.B., Sundberg J.P., and King L.E. Increased epidermal growth factor receptor in fsn/fsn mice. J. Invest. Dermatol. 106 (1996) 1169-1174
9. Werner S., Peters K.G., Longaker M.T., Fuller-Pace F., Banda M.J., and Williams L.T. Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 6896-6900
10. Grose R., and Werner S. An aPPArently protective mechanism for keratinocytes in wounded skin. Trends Mol. Med. 8 (2002) 149-151
11. Hoffmann J., Twiesselmann C., Kummer M.P., Romagnoli P., and Herzog V. A possible role for the Alzheimer amyloid precursor protein in the regulation of epidermal basal cell proliferation. Eur. J. Cell Biol. 79 (2000) 905-914
12. Siemes C., Quast T., Klein E., Bieber T., Hooper N.M., and Herzog V. Normalized proliferation of normal and psoriatic keratinocytes by suppression of alpha-secretase. J. Invest. Dermatol. 123 (2004) 556-563
13. Kirfel G., Borm B., Rigort A., and Herzog V. The secretory beta-amyloid precursor protein is a motogen for human epidermal keratinocytes. Eur. J. Cell Biol. 81 (2002) 664-676
14. Quast T., Wehner S., Kirfel G., Jaeger K., De Luca M., and Herzog V. sAPP as a regulator of dendrite motility and melanin release in epidermal melanocytes and melanoma cells. FASEB J. 17 (2003) 1739-1741
15. Sandbrink R., Masters C.L., and Beyreuther K. Beta A4-amyloid protein precursor mRNA isoforms without exon 15 are ubiquitously expressed in rat tissues including brain, but not in neurons. J. Biol. Chem. 269 (1994) 1510-1517
16. Paliga K., Peraus G., Kreger S., Durrwang U., Hesse L., Multhaup G., Masters C.L., Beyreuther K., and Weidemann A. Human amyloid precursor-like protein 1-cDNA cloning, ectopic expression in COS-7 cells and identification of soluble forms in the cerebrospinal fluid. Eur. J. Biochem. 250 (1997) 354-363
17. Slunt H.H., Thinakaran G., Von Koch C., Lo A.C., Tanzi R.E., and Sisodia S.S. Expression of a ubiquitous, cross-reactive homologue of the mouse beta-amyloid precursor protein (APP). J. Biol. Chem. 269 (1994) 2637-2644
18. Lorent K., Overbergh L., Moechars D., De Strooper B., Van Leuven F., and Van den Berghe H. Expression in mouse embryos and in adult mouse brain of three members of the amyloid precursor protein family, of the alpha-2-macroglobulin receptor/low density lipoprotein receptor-related protein and of its ligands apolipoprotein E, lipoprotein lipase, alpha-2-macroglobulin and the 40,000 molecular weight receptor-associated protein. Neuroscience 65 (1995) 1009-1025
19. Herzog V., Kirfel G., Siemes C., and Schmitz A. Biological roles of APP in the epidermis. Eur. J. Cell Biol. 83 (2004) 613-624
20. Rossjohn J., Cappai R., Feil S.C., Henry A., McKinstry W.J., Galatis D., Hesse L., Multhaup G., Beyreuther K., Masters C.L., and Parker M.W. Crystal structure of the N-terminal, growth factor-like domain of Alzheimer amyloid precursor protein. Nat. Struct. Biol. 6 (1999) 327-331
21. Cao X., and Sudhof T.C. A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293 (2001) 115-120
22. Schubert D., LaCorbiere M., Saitoh T., and Cole G. Characterization of an amyloid beta precursor protein that binds heparin and contains tyrosine sulfate. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 2066-2069
23. Narindrasorasak S., Altman R.A., Gonzalez-DeWhitt P., Greenberg B.D., and Kisilevsky R. An interaction between basement membrane and Alzheimer amyloid precursor proteins suggests a role in the pathogenesis of Alzheimer's disease. Lab. Invest. 72 (1995) 272-282
24. Narindrasorasak S., Lowery D.E., Altman R.A., Gonzalez-DeWhitt P.A., Greenberg B.D., and Kisilevsky R. Characterization of high affinity binding between laminin and Alzheimer's disease amyloid precursor proteins. Lab. Invest. 67 (1992) 643-652
25. Beher D., Hesse L., Masters C.L., and Multhaup G. Regulation of amyloid protein precursor (APP) binding to collagen and mapping of the binding sites on APP and collagen type I. J. Biol. Chem. 271 (1996) 1613-1620
26. Multhaup G., Schlicksupp A., Hesse L., Beher D., Ruppert T., Masters C.L., and Beyreuther K. The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 271 (1996) 1406-1409
27. Kamal A., Almenar-Queralt A., LeBlanc J.F., Roberts E.A., and Goldstein L.S. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414 (2001) 643-648
28. Lazarov O., Morfini G.A., Lee E.B., Farah M.H., Szodorai A., DeBoer S.R., Koliatsos V.E., Kins S., Lee V.M., Wong P.C., Price D.L., Brady S.T., and Sisodia S.S. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J. Neurosci. 25 (2005) 2386-2395
29. Li Z.W., Stark G., Gotz J., Rulicke T., Gschwind M., Huber G., Muller U., and Weissmann C. Generation of mice with a 200-kb amyloid precursor protein gene deletion by Cre recombinase-mediated site-specific recombination in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 6158-6162
30. Zheng H., Jiang M., Trumbauer M.E., Sirinathsinghji D.J., Hopkins R., Smith D.W., Heavens R.P., Dawson G.R., Boyce S., Conner M.W., Stevens K.A., Slunt H.H., Sisodia S.S., Chen H.Y., and Van der Ploeg L.H. beta-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81 (1995) 525-531
31. Muller U., Cristina N., Li Z.W., Wolfer D.P., Lipp H.P., Rulicke T., Brandner S., Aguzzi A., and Weissmann C. Behavioral and anatomical deficits in mice homozygous for a modified beta-amyloid precursor protein gene. Cell 79 (1994) 755-765
32. Tremml P., Lipp H.P., Muller U., Ricceri L., and Wolfer D.P. Neurobehavioral development, adult openfield exploration and swimming navigation learning in mice with a modified beta-amyloid precursor protein gene. Behav. Brain Res. 95 (1998) 65-76
33. von Koch C.S., Zheng H., Chen H., Trumbauer M., Thinakaran G., van der Ploeg L.H., Price D.L., and Sisodia S.S. Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol. Aging 18 (1997) 661-669
34. Heber S., Herms J., Gajic V., Hainfellner J., Aguzzi A., Rulicke T., von Kretzschmar H., von Koch C., Sisodia S., Tremml P., Lipp H.P., Wolfer D.P., and Muller U. Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20 (2000) 7951-7963
35. Parvathy S., Hussain I., Karran E.H., Turner A.J., and Hooper N.M. Alzheimer's amyloid precursor protein alpha-secretase is inhibited by hydroxamic acid-based zinc metalloprotease inhibitors: similarities to the angiotensin converting enzyme secretase. Biochemistry 37 (1998) 1680-1685
36. Caille I., Allinquant B., Dupont E., Bouillot C., Langer A., Muller U., and Prochiantz A. Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development 131 (2004) 2173-2181
37. Pietrzik C.U., Hoffmann J., Stober K., Chen C.Y., Bauer C., Otero D.A., Roch J.M., and Herzog V. From differentiation to proliferation: the secretory amyloid precursor protein as a local mediator of growth in thyroid epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 1770-1775
38. Gratzner H.G. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218 (1982) 474-475
39. Dombrowski F., Klotz L., Hacker H.J., Li Y., Klingmuller D., Brix K., Herzog V., and Bannasch P. Hyperproliferative hepatocellular alterations after intraportal transplantation of thyroid follicles. Am. J. Pathol. 156 (2000) 99-113
40. Hinz B., Alt W., Johnen C., Herzog V., and Kaiser H.W. Quantifying lamella dynamics of cultured cells by SACED, a new computer-assisted motion analysis. Exp. Cell Res. 251 (1999) 234-243
41. Caldelari R., Suter M.M., Baumann D., De Bruin A., and Muller E. Long-term culture of murine epidermal keratinocytes. J. Invest. Dermatol. 114 (2000) 1064-1065
42. Wehner S., Siemes C., Kirfel G., and Herzog V. Cytoprotective function of sAppalpha in human keratinocytes. Eur. J. Cell Biol. 83 (2004) 701-708
43. Popp G.M., Graebert K.S., Pietrzik C.U., Rosentreter S.M., Lemansky P., and Herzog V. Growth regulation of rat thyrocytes (FRTL-5 cells) by the secreted ectodomain of beta-amyloid precursor-like proteins. Endocrinology 137 (1996) 1975-1983
44. Condeelis J. Life at the leading edge: the formation of cell protrusions. Annu. Rev. Cell Biol. 9 (1993) 411-444
45. Soba P., Eggert S., Wagner K., Zentgraf H., Siehl K., Kreger S., Lower A., Langer A., Merdes G., Paro R., Masters C.L., Muller U., Kins S., and Beyreuther K. Homo- and heterodimerization of APP family members promotes intercellular adhesion. EMBO J. 25 (2005) 3624-3634
46. Kummer C., Wehner S., Quast T., Werner S., and Herzog V. Expression and potential function of beta-amyloid precursor proteins during cutaneous wound repair. Exp. Cell Res. 280 (2002) 222-232
47. Li Q., and Sudhof T.C. Cleavage of amyloid-beta precursor protein and amyloid-beta precursor-like protein by BACE 1. J. Biol. Chem. 279 (2004) 10542-10550
48. Werner S. Keratinocyte growth factor: a unique player in epithelial repair processes. Cytokine Growth Factor Rev. 9 (1998) 153-165
49. Ray P., Devaux Y., Stolz D.B., Yarlagadda M., Watkins S.C., Lu Y., Chen L., Yang X.F., and Ray A. Inducible expression of keratinocyte growth factor (KGF) in mice inhibits lung epithelial cell death induced by hyperoxia. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6098-6103
50. Guo L., Degenstein L., and Fuchs E. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 10 (1996) 165-175
51. Kirfel G., and Herzog V. Migration of epidermal keratinocytes: mechanisms, regulation, and biological significance. Protoplasma 223 (2004) 67-78