The α isoform of protein kinase C is involved in signaling the response of desmosomes to wounding in cultured epithelial cells

Molecular Biology of the Cell

Volumn 11, Issue 3, 2000, Pages 1077-1092

  Wallis, Sarah ^a,c   Lloyd, Susan ^b,d   Wise, Irene ^a   Ireland, Grenham ^a   Fleming, Tom P ^b   Garrod, David ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c Unipath   (United Kingdom)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CALCIUM; ISOENZYME; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DAMAGE; CONTROLLED STUDY; DESMOSOME; ENZYME ACTIVATION; ENZYME LOCALIZATION; EPITHELIUM CELL; EPITHELIZATION; MONOLAYER CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0034020357     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.3.1077     Document Type: Article

References (75)

1. Abraham, J.A., and Klagsbrun, M. (1996). Modulation of wound repair by members of the fibroblast growth factor family. In: The Molecular and Cellular Biology of Wound Repair, 2nd ed., ed. R.A.F. Clark, New York: Plenum Press, 195-248.
2. Armstrong, D.K., McKenna, K.E., Purkis, P.E., Green, K.J., Eady, R.A., Leigh, I.M., and Hughes, A.E. (1999). Haploinsufficiency of desmoplakin causes a striate subtype of palmoplantar keratoderma. Hum. Mol. Genet. 8, 143-148.
3. Balda, M.S.L., Gonzalez-Marriscal, R.G., Contreras, M., Marcias-Silva, M.E., Torres-Marquez, J.A., and Cereijido, M. (1991). Assembly and sealing of tight junctions: possible participation of G-proteins, phospholipase C, protein kinase C and calmodulin. J. Membr. Biol. 122, 193-202.
4. Baribault, H., Blouin, R., Bourgon, L., and Marceau, N. (1989). Epidermal growth factor-induced selective phosphorylation of cultured rat hepatocyte 55-kD cytokeratin before filament reorganization and DNA synthesis. J. Cell Biol. 109, 1665-1676.
5. Bierkamp, C., McLaughlin, K.J., Schwartz, H., Huber, O., and Kemler, R. (1996). Embryonic heart and skin defects in mice lacking plakoglobin. Dev. Biol. 180, 780-785.
6. Bornslaeger, E.A., Corcoran, CM., Stappenbeck, T.S., and Green, K.J. (1996). Breaking the connection: displacement of the desmosomal plaque protein desmoplakin from cell-cell interfaces disrupts anchorage of intermediate filament bundles and alters intercellular junction assembly. J. Cell Biol. 234, 985-1001.
7. Borysenko, J.Z., and Revel, J.P. (1973). Experimental manipulation of desmosome structure. J. Anat. 337, 403-422.
8. Brandner, J.M., Reidenbach, S., and Franke, W.W. (1997). Evidence that "pinin," reportedly a differentiation specific desmosomal protein, is actually a widespread nuclear protein. Differentiation 62, 119-127.
9. Brock, J., Midwinter, K., Lewis, J., and Martin, P. (1996). Healing of incisional wounds in the embryonic chick wing bud: characterization of the action purse-string and demonstration of the requirement for Rho activation. J. Cell Biol. 335, 1097-1107.
10. Charles, A.C., Naus, C.C., Zhu, D., Kidder, G.M., Dirksen, E.R., and Sanderson, M.J. (1992). Intercellular calcium signaling via gap junctions in glioma cells. J. Cell Biol. 118, 195-201.
11. ++-dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollin, contributes to cell-cell adhesion. J. Cell Biol. 338, 193-201.
12. Colledge, M., and Scott, J.D. (1999). AKAPs: from structure to function. Trends Cell Biol. 9, 216-221.
13. Collins, J.E., Taylor, I., and Garrod, D.R. (1990). A study of desmosomes in colorectal carcinoma. Br. J. Cancer 62, 796-805.
14. Cowell, H.E., and Garrod, D.R. (1999). Activation of protein kinase C modulates cell-cell and cell-substratum adhesion of a human colorectal carcinoma cell line, and restores normal epithelial morphology. Int. J. Cancer 80, 455-464.
15. Dong, L., Stevens, J.L., and Jaken, S. (1993). Transformation-sensitive localization of α-protein kinase C at cell-cell contacts in rat renal proximal epithelial cells. Cell Growth Differ. 4, 793-798.
16. Duden, R., and Franke, W.W. (1988). Organization of desmosomal plaque proteins in cells growing at low calcium concentration. J. Cell Biol. 107, 375-412.
17. Dustin, M.L., and Springer, T.A. (1989). T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 343, 619-624.
18. Dwyer-Nield, L.D., Miller, A.C.K., Neighbors, B.W., Dinsdale, D., and Malkinson, A.M. (1996). Cytoskeletal architecture in mouse lung epithelial cells is regulated by protein kinase C-α and calpain II. Am. J. Physiol. 270, L526-L534.
19. Ealey, P.A., Yatesman, M.E., Holt, S.J., and Marshall, N.J. (1988). ESTA: a bioassay system for the determination of the potencies of hormones and antibodies which mimic their action. J. Mol. Endocrinol. 1, R1-R4.
20. Eger, A., Stockinger, A., Wiche, G., and Foisner, R. (1997). Polarisation-dependent association of lectin with desmoplakin and the lateral submembrane skeleton in MDCK cells. J. Cell Sci. 770, 1307-1316.
21. Garrod, D.R., Tselepis, C., Runswick, S., North, A.J., Wallis, S.R., and Chidgey, M.A.J. (1999). Desmosomal adhesion. In: The Adhesive Interactions of Cells, ed. D.R. Garrod, M.A.J. Chidgey, A.J. North, Greenwich, CT: JAI Press, 165-201.
22. Godson, C., Bell, K.S., and Insel, P.A. (1993). Inhibition of expression of protein kinase C alpha by antisense cDNA inhibits phorbol ester-mediated arachidonate release. J. Biol. Chem. 268, 11946-11950.
23. ++ induced and phorbolester-stabilized membrane binding of protein kinase C. J. Biol. Chem. 261, 16438-16445.
24. Gott, A.L., Mallon, B.S., Paton, A., Groome, N., and Rumsby, M.G. (1994). Rat brain glial cells in primary culture and subculture contain the delta, epsilon and zeta subspecies of protein kinase C as well as the conventional subspecies. Neurosci. Lett. 171, 117-120.
25. Guo, L., Degenstein, L., Dowling, J., Yu, Q.C., Wollmann, R., Perman, B., and Fuchs, E. (1995). Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell 81, 233-243.
26. Hennings, H., and Holbrook, K.A. (1983). Calcium regulation of cell-cell contact and differentiation of epidermal cells in culture: an ultrastructural study. Exp. Cell Res. 743, 127-142.
27. Kartenbeck, J., Schmid, E., Franke, W.W., and Geiger, B. (1982). Different modes of internalization of proteins associated with adherens junctions and of the desmosomal plaque material. EMBO J. 1, 725-732.
28. Kitajima, Y., Inoue, S., Nagao, S., Nagtata, K., Yaoita, H., and Nozawa, Y. (1988). Biphasic effects of 12-O-tetradecanoyl-phorbol-13-acetate on the cell morphology of low calcium human epidermal carcinoma cells: involvement of translocation and down regulation of protein kinase C. Cancer Res. 48, 964-970.
29. Kouklis, P.D., Hutton, E., and Fuchs, E. (1994). Making a connection: direct binding between keratin intermediate filaments and desmosomal proteins. J. Cell Biol. 727, 1049-1060.
30. Kowalczyk, A.P., Bornslaeger, E.A., Borgwardt, J.E., Palka, H.L., Dhaliwal, A.S., Corcoran, C.M., Denning, M.F., and Green, K.J. (1997). The amino-terminal domain of desmoplakin binds to plako-globin and clusters desmosomal cadherin-plakoglobin complexes. J. Cell Biol. 139, 773-784.
31. Ku, N.-O., and Omary, M.B. (1994). Identification of the major physiologic phosphorylation site of human keratin 18: potential kinase and a role in filament reorganization. J. Cell Biol. 727, 161-171.
32. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
33. Laudanna, C., Mochly-Rosen, D., Litov, T., Constantin, G., and Butcher, E.C. (1998). Evidence of ζ protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J. Biol. Chem. 273, 30306-30315.
34. Liao, L., and Jaken, S. (1993). Effect of α-protein kinase C neutralizing antibodies and the pseudosubstrate peptide on phosphorylation, migration, and growth of REF-52 cells. Cell Growth Differ. 4, 309-316.
35. Lin, N., and Bazan, H.E. (1995). Protein kinase C substrates in corneal epithelium during wound healing: the phosphorylation of growth associated protein-43 (GAP-43). Exp. Eye Res. 61, 451-459.
36. Marcozzi, C., Burdctt, I.D.J., Buxton, R.S., and Magee, A.I. (1998). Expression of both types of desmosomal cadherins and plakoglobin confers strong intercellular adhesion. J. Cell Sci. 171, 495-509.
37. Marikovsky, M., Breuing, K., Liu, P.Y., Eriksson, E., Higashiyama, S., Farber, P., Abraham, J., and Klagsbrun, M. (1993). Appearance of heparin-binding EGF-like growth factor in wound fluid as a response to injury. Proc. Natl. Acad. Sci. USA 90, 3889-3893.
38. Martin, P. (1997). Wound healing: aiming for perfect skin regeneration. Science 276, 75-81.
39. Martiny-Baron, G., Kazanietz, M.G., Mischak, H., Blumberg, P.M., Kochs,'G., Hig, H., Marme, D., and Schachtele, C. (1993). Selective inhibition of protein kinase C isozymes by the indolocarbazole G56976. J. Biol. Chem. 268, 9194-9197.
40. Mattey, D.L., and Garrod, D.R. (1986a). Calcium-induced desmosome formation in cultured kidney epithelial cells. J. Cell Sci. 85, 95-111.
41. Mattey, D.L., and Garrod, D.R. (1986b). Splitting and internalization of the desmosome of cultured kidney epithelial cells by reduction in calcium concentrations. J. Cell Sci. 85, 113-124.
42. McGrath, J.A., McMillan, J.R., Shemanko, CS., Runswick, S.K., Leigh, I.M., Lane, E.B., Garrod, D.R., and Eady, AJ. (1997). Mutations in the plakophilin 1 gene result in ectodermal dysplasia/skin fragility syndrome. Nat. Genet. 17, 240-244.
43. Mochly-Rosen, D. (1995). Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 268, 247-251.
44. Montesano, R., Schaller, G., and Orci, L. (1991). Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697-711.
45. Nanney, L.B., and King, L.E. (1996). Epidermal growth factor and transforming growth factor-α. In: The Molecular and Cellular Biology of Wound Repair, 2nd ed., ed. R.A.F. Clark, New York: Plenum Press, 171-194.
46. North, A.J., Chidgey, M.A., Clarke, J.P., Bardsley, W.G., and Garrod, D.R. (1996). Distinct desmocollin isoforms occur in the same desmosomes and show reciprocally graded distributions in bovine nasal epidermis. Proc. Natl. Acad. Sci. USA 93, 7701-7705.
47. Osada, K., Seishima, M., and Kitajama, Y. (1997). Pemphigus IgG activates and translocates protein kinase C from the cytosol to the particulate/cytoskeleton fraction in human keratinocytes. J. Invest. Dermatoi. 108, 482-487.
48. Ouyang, P., and Sugrue, S.P. (1992). Identification of an epithelial protein related to the desmosome and intermediate filament network. J. Cell Biol. 118, 1477-1488.
49. Ouyang, P., and Sugrue, S.P. (1996). Characterization of pinin, a novel protein associated with the desmosome-intermediate filament complex. J. Cell Biol. 135, 1027-1042.
50. Paladini, R.D., Takahachi, K., Bravo, N.S., and Coulombe, P.A. (1996). Onset of re-epithelialization after skin injury correlates with a re-organization of keratin filaments in wound edge keratinocytes: defining a potential role for keratin 16. J. Cell Biol. 132, 381-397.
51. Parrish, E.P., Steart, P.V., Garrod, D.R., and Weller, R.O. (1987). Antidesmosomal monoclonal antibody in the diagnosis of intracranial tumors. J. Pathol. 153, 265-273.
52. Pasdar, M., Li, Z., and Chan, H. (1992). Desmosome assembly in MDCK epithelial cells does not require the presence of functional microtubules. Cell Motil. Cytoskeleton 23, 201-212.
53. Rickman, L., et al. (1999). N-terminal deletion in a desmosomal cadherin causes the autosomal dominant skin disease striate palmo-planter keratoderma. Hum. Mol. Genet. 8, 971-976.
54. Romer, J., Bugge, T.H., Pyke, C., Lund, L.R., Flick, M.J., Degen, J.L., and Dano, K. (1996). Impaired wound healing in mice with a disrupted plasminogen gene. Nat. Med. 2, 287-292.
55. Ruiz, P., et al. (1996). Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J. Cell Biol. 335, 215-225.
56. Saarialho-Kere, U.K., Chang, E.S., VVelgus, H.G., and Parks, W.C. (1992). Distinct localization of collagenase and tissue inhibitor matalloproteinases: expression in wound healing associated with ulcerative pyogenic granuloma. J. Clin. Invest. 90, 1952-1957.
57. Saarialho-Kere, U.K., Pentland, A.P., Birkedal-Hansen, H., Parks, W.C., and Welgus, H.G. (1994). Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds. J. Clin. Invest. 94, 79-88.
58. Salo, T., Makela, M., Kylmaniemi, M., Autio-Harmainen, H., and Larjava, H. (1994). Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab. Invest. 70, 176-182.
59. Shea, T.B., Beermann, M.L., Griffin, W.R., and Leli, U. (1994). Degradation of protein kinase Cα and its free catalytic subunit, protein kinase M, in intact human neuroblastoma cells and under cell-free conditions. FEBS Lett. 350, 223-229.
60. Sheu, H.M., Kitajama, Y., and Yaoita, H. (1989). Involvement of protein kinase C in translocation of desmoplakins from cytosol to plasma membrane during desmosome formation in human squamous cell carcinoma cells grown in low and normal calcium concentration. Exp. Cell Res. 185, 176-190.
61. Shirayoshi, Y., Nose, A., Iwasaki, K., and Takeichi, M. (1986). N-linked oligosaccharides are not involved in the function of cell-cell binding protein E-cadherin. Cell Struct. Funct. 11, 245-252.
62. Smith, E.A., and Fuchs, E. (1998). Defining the interactions between intermediate filaments and desmosomes. J. Cell Biol. 242, 1229-1241.
63. Sneyd, J., Charles, A.C., and Sanderson, M.J. (1994). A model for the propagation of intercellular calcium waves. Am. J. Physiol. 33, C293-C302.
64. Stabel, S., and Parker, P.J. (1991). Protein kinase C. Pharmacol. Ther. 52, 71-95.
65. Stappenbeck, T.S., and Green, K.J. (1992). The desmoplakin carboxyl terminus coaligns with and specifically disrupts intermediate filament networks when expressed in cultured cells. J. Cell Biol. 116, 1197-1209.
66. Stevenson, B.R., Siliciano, J.D., Mooseker, M.S., and Goodenough, D.A. (1986). Identification of ZO-1: a high molecular weight polypeptide associated with tight junction (zonula ocludens) in a variety of epithelia. J. Cell Biol. 103, 755-766.
67. Stoker, M., Gherardi, E., Perryman, M., and Gray, J. (1987). Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature 238, 238-242.
68. Tselepis, C., Chidgey, M.A.J., North, A.J., and Garrod, D.R. (1998). Desmosomal adhesion inhibits invasive behavior. Proc. Natl. Acad. Sci. USA 95, 8064-8069.
69. van Hengel, J., Gohon, L., Bruyneel, E., Vermeulen, S., Cornelissen, M., Mareel, M., and van Roy, F. (1997). Protein kinase C activation upregulates intercellular adhesion of α-catenin-negative human colon cancer cell variants via induction of desmosomes. J. Cell Biol. 737, 1103-1116.
70. Vestweber, D., and Kemler, R. (1985). Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 4, 3393-3398.
71. Vuori, K., and Ruoslahti, E. (1993). Activation of protein kinase C precedes α5β1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268, 21459-21462.
72. Wacker, I.U., Rickard, J.E., De Mey, J.R., and Kreis, T.E. (1992). Accumulation of a microtubule-binding protein, pp170, at desmosomal plaques. J. Cell Biol. 217, 813-824.
73. Watt, F.M., Mattey, D.L., and Garrod, D.R. (1984). Calcium-induced reorganisation of desmosomal components in cultured human keratinocytes. J. Cell Biol. 99, 2211-2215.
74. Woods, A., and Couchman, J.R. (1992). Protein kinase C involvement in focal adhesion formation. J. Cell Sci. 101, 277-290.
75. Yano, T., Tokui, T., Nishi, Y., Nishizawa, K., Shibata, K., Kikuchi, K., Tsuiki, S., Yamauchi, T., and Inagaki, M. (1991). Phosphorylation of keratin intermediate filaments by protein kinase C, by calmodulin-dependent protein kinase and by cAMP-dependent protein kinase. Eur. J. Biochem. 297, 281-290.