Disruption of spectrin-like cytoskeleton in differentiating keratinocytes by PKCδ activation is associated with phosphorylated adducin

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Zhao, Kong Nan ^a,c   Masci, Paul P ^b   Lavin, Martin F ^a,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADDUCIN; ANTIMITOTIC AGENT; PROTEIN KINASE C; SMALL INTERFERING RNA; SPECTRIN; THREONINE; ACTIN; CALMODULIN BINDING PROTEIN; PROTEIN KINASE C DELTA;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; EPIDERMIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; KERATINOCYTE; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; CYTOPLASM; GENETIC PROCEDURES; GENETICS; METABOLISM; MICROTUBULE; PHOSPHORYLATION; SKIN;

ACTINS; ANIMALS; CALMODULIN-BINDING PROTEINS; CELLS, CULTURED; CYTOPLASM; CYTOSKELETON; GENETIC TECHNIQUES; HUMANS; KERATINOCYTES; MICE; MICROTUBULES; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; RNA, SMALL INTERFERING; SKIN; SPECTRIN;

EID: 82855168067     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028267     Document Type: Article

References (77)

1. Pinder JC, Baines AJ, (2000) A protein accumulator. Nature 406: 253-254.
2. Bennett V, Healy J, (2008) Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol Med 14: 28-36.
3. Steck TL, (1974) The organization of proteins in the human red blood cell membrane. A review. J Cell Biol 62: 1-19.
4. Painter RG, Sheetz M, Singer SJ, (1975) Detection and ultrastructural localization of human smooth muscle myosin-like molecules in human non-muscle cells by specific antibodies. Proc Natl Acad Sci U S A 72: 1359-1363.
5. Hiller G, Weber K, (1977) Spectrin is absent in various tissue culture cells. Nature 266: 181-183.
6. Goodman SR, Zagon IS, Kulikowski RR, (1981) Identification of a spectrin-like protein in nonerythroid cells. Proc Natl Acad Sci U S A 78: 7570-7574.
7. Granger BL, Lazarides E, (1985) Appearance of new variants of membrane skeletal protein 4.1 during terminal differentiation of avian erythroid and lenticular cells. Nature 313: 238-241.
8. Repasky EA, Granger BL, Lazarides E, (1982) Widespread occurrence of avian spectrin in nonerythroid cells. Cell 29: 821-833.
9. Hassoun H, Vassiliadis JN, Murray J, Yi SJ, Hanspal M, et al. (1995) Molecular basis of spectrin deficiency in beta spectrin Durham. A deletion within beta spectrin adjacent to the ankyrin-binding site precludes spectrin attachment to the membrane in hereditary spherocytosis. J Clin Invest 96: 2623-2629.
10. Hammarlund M, Davis WS, Jorgensen EM, (2000) Mutations in beta-spectrin disrupt axon outgrowth and sarcomere structure. J Cell Biol 149: 931-942.
11. Moorthy S, Chen L, Bennett V, (2000) Caenorhabditis elegans beta-G spectrin is dispensable for establishment of epithelial polarity, but essential for muscular and neuronal function. J Cell Biol 149: 915-930.
12. Dubreuil RR, Wang P, Dahl S, Lee J, Goldstein LS, (2000) Drosophila beta spectrin functions independently of alpha spectrin to polarize the Na,K ATPase in epithelial cells. J Cell Biol 149: 647-656.
13. Toulza E, Mattiuzzo NR, Galliano MF, Jonca N, Dossat C, et al. (2007) Large-scale identification of human genes implicated in epidermal barrier function. Genome Biol 8: R107.
14. Fuchs E, Raghavan S, (2002) Getting under the skin of epidermal morphogenesis. Nat Rev Genet 3: 199-209.
15. Eckert RL, Crish JF, Robinson NA, (1997) The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation. Physiol Rev 77: 397-424.
16. Fuchs E, (2007) Scratching the surface of skin development. Nature 445: 834-842.
17. Kariniemi AL, Lehto VP, Virtanen I, (1984) Distribution of p230, an alpha-spectrin-related polypeptide in normal and psoriatic epidermis and in cultured human keratinocytes. Br J Dermatol 111: 139-145.
18. Tuominen H, Sormunen R, Kallioinen M, (1996) Non-erythroid spectrin (fodrin) in cutaneous tumours: diminished in cell membranes, increased in the cytoplasm. Br J Dermatol 135: 576-580.
19. Zhao KN, Gu W, Fang NX, Saunders NA, Frazer IH, (2005) Gene codon composition determines differentiation-dependent expression of a viral capsid gene in keratinocytes in vitro and in vivo. Mol Cell Biol 25: 8643-8655.
20. Fang NX, Gu W, Ding J, Saunders NA, Frazer IH, et al. (2007) Calcium enhances mouse keratinocyte differentiation in vitro to differentially regulate expression of papillomavirus authentic and codon modified L1 genes. Virology 365: 187-197.
21. Silvestre JS, Thery C, Hamard G, Boddaert J, Aguilar B, et al. (2005) Lactadherin promotes VEGF-dependent neovascularization. Nature medicine 11: 499-506.
22. Li B, Wang X, Zhou F, Saunders NA, Frazer IH, et al. (2008) Up-regulated expression of Sp1 protein coincident with a viral protein in human and mouse differentiating keratinocytes may act as a cell differentiation marker. Differentiation 76: 1068-1080.
23. Lewis L, Barrandon Y, Green H, Albrecht-Buehler G, (1987) The reorganization of microtubules and microfilaments in differentiating keratinocytes. Differentiation 36: 228-233.
24. Lechler T, Fuchs E, (2007) Desmoplakin: an unexpected regulator of microtubule organization in the epidermis. J Cell Biol 176: 147-154.
25. Weil M, Raff MC, Braga VM, (1999) Caspase activation in the terminal differentiation of human epidermal keratinocytes. Curr Biol 9: 361-364.
26. Shimizu T, Takakuwa Y, Koizumi H, Ishibashi T, Ohkawara A, (1995) Localization of immuno-analogues of erythrocyte protein 4.1 and spectrin in epidermis of psoriasis vulgaris. Histochem Cell Biol 103: 363-368.
27. Holland P, Willis C, Kanaly S, Glaccum M, Warren A, et al. (2002) RIP4 is an ankyrin repeat-containing kinase essential for keratinocyte differentiation. Curr Biol 12: 1424-1428.
28. Aho S, Buisson M, Pajunen T, Ryoo YW, Giot JF, et al. (2000) Ubinuclein, a novel nuclear protein interacting with cellular and viral transcription factors. J Cell Biol 148: 1165-1176.
29. Lux SE, John KM, Bennett V, (1990) Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature 344: 36-42.
30. Lux SE, Tse WT, Menninger JC, John KM, Harris P, et al. (1990) Hereditary spherocytosis associated with deletion of human erythrocyte ankyrin gene on chromosome 8. Nature 345: 736-739.
31. Dlugosz AA, Mischak H, Mushinski JF, Yuspa SH, (1992) Transcripts encoding protein kinase C-alpha,-delta,-epsilon,-zeta, and-eta are expressed in basal and differentiating mouse keratinocytes in vitro and exhibit quantitative changes in neoplastic cells. Mol Carcinog 5: 286-292.
32. Johansen C, Iversen L, Ryborg A, Kragballe K, (2000) 1alpha,25-dihydroxyvitamin D3 induced differentiation of cultured human keratinocytes is accompanied by a PKC-independent regulation of AP-1 DNA binding activity. J Invest Dermatol 114: 1174-1179.
33. Stanwell C, Denning MF, Rutberg SE, Cheng C, Yuspa SH, et al. (1996) Staurosporine induces a sequential program of mouse keratinocyte terminal differentiation through activation of PKC isozymes. J Invest Dermatol 106: 482-489.
34. Rutberg SE, Saez E, Glick A, Dlugosz AA, Spiegelman BM, et al. (1996) Differentiation of mouse keratinocytes is accompanied by PKC-dependent changes in AP-1 proteins. Oncogene 13: 167-176.
35. Lee YS, Dlugosz AA, McKay R, Dean NM, Yuspa SH, (1997) Definition by specific antisense oligonucleotides of a role for protein kinase C alpha in expression of differentiation markers in normal and neoplastic mouse epidermal keratinocytes. Mol Carcinog 18: 44-53.
36. Deucher A, Efimova T, Eckert RL, (2002) Calcium-dependent involucrin expression is inversely regulated by protein kinase C (PKC)alpha and PKCdelta. J Biol Chem 277: 17032-17040.
37. Parekh D, Ziegler W, Yonezawa K, Hara K, Parker PJ, (1999) Mammalian TOR controls one of two kinase pathways acting upon nPKCdelta and nPKCepsilon. J Biol Chem 274: 34758-34764.
38. Liedtke CM, Hubbard M, Wang X, (2003) Stability of actin cytoskeleton and PKC-delta binding to actin regulate NKCC1 function in airway epithelial cells. Am J Physiol Cell Physiol 284: C487-496.
39. Nestor MW, Cai X, Stone MR, Bloch RJ, Thompson SM, (2011) The actin binding domain of betaI-spectrin regulates the morphological and functional dynamics of dendritic spines. PLoS One 6: e16197.
40. Morton WM, Ayscough KR, McLaughlin PJ, (2000) Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol 2: 376-378.
41. Fan Y, Zhang YQ, Sun DJ, Zhang YN, Wu XW, et al. (2009) Rottlerin protected dopaminergic cell line from cytotoxicity of 6-hydroxydopamine by inhibiting PKCdelta phosphorylation. Neurosci Bull 25: 187-195.
42. Gardner K, Bennett V, (1987) Modulation of spectrin-actin assembly by erythrocyte adducin. Nature 328: 359-362.
43. Gilligan DM, Sarid R, Weese J, (2002) Adducin in platelets: activation-induced phosphorylation by PKC and proteolysis by calpain. Blood 99: 2418-2426.
44. Peters LL, White RA, Birkenmeier CS, Bloom ML, Lux SE, et al. (1992) Changing patterns in cytoskeletal mRNA expression and protein synthesis during murine erythropoiesis in vivo. Proc Natl Acad Sci U S A 89: 5749-5753.
45. Li X, Bennett V, (1996) Identification of the spectrin subunit and domains required for formation of spectrin/adducin/actin complexes. J Biol Chem 271: 15695-15702.
46. Kaiser HW, Ness W, O'Keefe E, Balcerkiewicz A, Kreysel HW, (1993) Localization of adducin in epidermis. J Invest Dermatol 101: 783-788.
47. Kariniemi AL, Holthofer H, Vartio T, Virtanen I, (1984) Cellular differentiation of basal cell carcinoma studied with fluorescent lectins and cytokeratin antibodies. J Cutan Pathol 11: 541-548.
48. Roop D, (1995) Defects in the barrier. Science 267: 474-475.
49. Mangeat PH, Burridge K, (1984) Immunoprecipitation of nonerythrocyte spectrin within live cells following microinjection of specific antibodies: relation to cytoskeletal structures. J Cell Biol 98: 1363-1377.
50. Sikorski AF, Sangerman J, Goodman SR, Critz SD, (2000) Spectrin (betaSpIIsigma1) is an essential component of synaptic transmission. Brain Res 852: 161-166.
51. De Matteis MA, Morrow JS, (2000) Spectrin tethers and mesh in the biosynthetic pathway. J Cell Sci 113 (Pt 13): 2331-2343.
52. Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, et al. (2002) Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416: 143-149.
53. Pines J, Hunter T, (1990) p34cdc2: the S and M kinase? New Biol 2: 389-401.
54. Banan A, Zhang LJ, Shaikh M, Fields JZ, Farhadi A, et al. (2004) Theta-isoform of PKC is required for alterations in cytoskeletal dynamics and barrier permeability in intestinal epithelium: a novel function for PKC-theta. Am J Physiol Cell Physiol 287: C218-234.
55. Manno S, Takakuwa Y, Nagao K, Mohandas N, (1995) Modulation of erythrocyte membrane mechanical function by beta-spectrin phosphorylation and dephosphorylation. J Biol Chem 270: 5659-5665.
56. Sihag RK, (1998) Brain beta-spectrin phosphorylation: phosphate analysis and identification of threonine-347 as a heparin-sensitive protein kinase phosphorylation site. J Neurochem 71: 2220-2228.
57. Perrotta S, del Giudice EM, Iolascon A, De Vivo M, Di Pinto D, et al. (2001) Reversible erythrocyte skeleton destabilization is modulated by beta-spectrin phosphorylation in childhood leukemia. Leukemia 15: 440-444.
58. Fowler VM, Adam EJ, (1992) Spectrin redistributes to the cytosol and is phosphorylated during mitosis in cultured cells. J Cell Biol 119: 1559-1572.
59. Baumann O, (1998) Association of spectrin with a subcompartment of the endoplasmic reticulum in honeybee photoreceptor cells. Cell motility and the cytoskeleton 41: 74-86.
60. Sato S, Jinbu Y, Nakao M, (1986) Characterization of human erythrocyte cytoskeletal ATPase. Journal of biochemistry 100: 643-649.
61. Hoben GM, Athanasiou KA, (2008) Use of staurosporine, an actin-modifying agent, to enhance fibrochondrocyte matrix gene expression and synthesis. Cell and tissue research 334: 469-476.
62. Khurana RN, Deng PF, Epstein DL, Vasantha RP, (2003) The role of protein kinase C in modulation of aqueous humor outflow facility. Experimental eye research 76: 39-47.
63. Ligon LA, Karki S, Tokito M, Holzbaur EL, (2001) Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nature cell biology 3: 913-917.
64. Gregorio CC, Repasky EA, Fowler VM, Black JD, (1994) Dynamic properties of ankyrin in T lymphocytes: colocalization with spectrin and protein kinase C beta. J Cell Biol 125: 345-358.
65. Zhu L, Brodie C, Balasubramanian S, Eckert RL, (2008) Multiple PKCdelta tyrosine residues are required for PKCdelta-dependent activation of involucrin expression-a key role of PKCdelta-Y311. J Invest Dermatol 128: 833-845.
66. Eckert RL, Crish JF, Efimova T, Dashti SR, Deucher A, et al. (2004) Regulation of involucrin gene expression. J Invest Dermatol 123: 13-22.
67. Efimova T, Broome AM, Eckert RL, (2004) Protein kinase Cdelta regulates keratinocyte death and survival by regulating activity and subcellular localization of a p38delta-extracellular signal-regulated kinase 1/2 complex. Mol Cell Biol 24: 8167-8183.
68. Adhikary G, Chew YC, Reece EA, Eckert RL, (2010) PKC-delta and-eta, MEKK-1, MEK-6, MEK-3, and p38-delta are essential mediators of the response of normal human epidermal keratinocytes to differentiating agents. J Invest Dermatol 130: 2017-2030.
69. Efimova T, Eckert RL, (2000) Regulation of human involucrin promoter activity by novel protein kinase C isoforms. J Biol Chem 275: 1601-1607.
70. Cerda SR, Mustafi R, Little H, Cohen G, Khare S, et al. (2006) Protein kinase C delta inhibits Caco-2 cell proliferation by selective changes in cell cycle and cell death regulators. Oncogene 25: 3123-3138.
71. Bennett V, Baines AJ, (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81: 1353-1392.
72. Matsuoka Y, Li X, Bennett V, (1998) Adducin is an in vivo substrate for protein kinase C: phosphorylation in the MARCKS-related domain inhibits activity in promoting spectrin-actin complexes and occurs in many cells, including dendritic spines of neurons. J Cell Biol 142: 485-497.
73. Kaiser HW, O'Keefe E, Bennett V, (1989) Adducin: Ca++-dependent association with sites of cell-cell contact. J Cell Biol 109: 557-569.
74. Barkalow KL, Italiano JE Jr, Chou DE, Matsuoka Y, Bennett V, et al. (2003) Alpha-adducin dissociates from F-actin and spectrin during platelet activation. J Cell Biol 161: 557-570.
75. George A, Pushkaran S, Li L, An X, Zheng Y, et al. (2010) Altered phosphorylation of cytoskeleton proteins in sickle red blood cells: the role of protein kinase C, Rac GTPases, and reactive oxygen species. Blood cells, molecules & diseases 45: 41-45.
76. Matsuoka Y, Li X, Bennett V, (2000) Adducin: structure, function and regulation. Cell Mol Life Sci 57: 884-895.
77. Tamaru S, Fukuta T, Kaibuchi K, Matsuoka Y, Shiku H, et al. (2005) Rho-kinase induces association of adducin with the cytoskeleton in platelet activation. Biochemical and biophysical research communications 332: 347-351.