Atypical protein kinase C in cell motility

Cellular and Molecular Life Sciences

Volumn 70, Issue 17, 2013, Pages 3057-3066

  Xiao, Helan ^a,b   Liu, Mingyao ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

Cell invasion; Cell migration; Invadopodia; Lamellipodia; MMP; Podosome

Indexed keywords

AQUAPORIN 9; CD34 ANTIGEN; CD38 ANTIGEN; GLYCOGEN SYNTHASE KINASE 3BETA; MATRIX METALLOPROTEINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN CDC42; PROTEIN KINASE C; PROTEIN KINASE C DELTA; PROTEIN KINASE C ZETA;

CANCER CELL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL ORGANELLE; CELL POLARIZATION; CELL TYPE; CELLULAR PARAMETERS; ENZYME ACTIVATION; ENZYME ACTIVITY; FILOPODIA; HEMATOPOIETIC CELL; HUMAN; INTRACELLULAR SIGNALING; INVADOPODIA; NONHUMAN; PODOSOME; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; STRUCTURE ACTIVITY RELATION;

ANIMALS; CELL MOVEMENT; HUMANS; NEOPLASMS; PROTEIN KINASE C;

EID: 84882454959     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1192-1     Document Type: Review

References (81)

1. Newton AC (2003) Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem J 370:361-371
2. Gonzalez-Guerrico AM, Meshki J, Xiao L, Benavides F, Conti CJ, Kazanietz MG (2005) Molecular mechanisms of protein kinase C-induced apoptosis in prostate cancer cells. J Biochem Mol Biol 38:639-645
3. Carter CA, Kane CJ (2004) Therapeutic potential of natural compounds that regulate the activity of protein kinase C. Curr Med Chem 11:2883-2902
4. de Barry J, Liegeois CM, Janoshazi A (2010) Protein kinase C as a peripheral biomarker for Alzheimer's disease. Exp Gerontol 45:64-69
5. Dempsey EC, Cool CD, Littler CM (2007) Lung disease and PKCs. Pharmacol Res 55:545-559
6. Harper MT, Poole AW (2010) Diverse functions of protein kinase C isoforms in platelet activation and thrombus formation. J Thromb Haemost 8:454-462
7. Gonelli A, Mischiati C, Guerrini R, Voltan R, Salvadori S, Zauli G (2009) Perspectives of protein kinase C (PKC) inhibitors as anti-cancer agents. Mini Rev Med Chem 9:498-509
8. Ali AS, Ali S, El-Rayes BF, Philip PA, Sarkar FH (2009) Exploitation of protein kinase C: a useful target for cancer therapy. Cancer Treat Rev 35:1-8
9. Tuttle KR (2008) Protein kinase C-beta inhibition for diabetic kidney disease. Diabetes Res Clin Pract 82(Suppl 1):S70-S74
10. Galvez MI (2009) Rubosixtaurin and other PKC inhibitors in diabetic retinopathy and macular edema. Review. Curr Diabetes Rev 5:14-17
11. Lang D, Beermann ML, Hauser G, Cressman CM, Shea TB (1995) Phospholipids inhibit proteolysis of protein kinase C alpha by mM calcium-requiring calpain. Neurochem Res 20:1361-1364
12. Parker PJ, Murray-Rust J (2004) PKC at a glance. J Cell Sci 117:131-132
13. Griner EM, Kazanietz MG (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat Rev Cancer 7:281-294
14. Vertommen D, Rider M, Ni Y, Waelkens E, Merlevede W, Vandenheede JR, Van Lint J (2000) Regulation of protein kinase D by multisite phosphorylation. Identification of phosphorylation sites by mass spectrometry and characterization by site-directed mutagenesis. J Biol Chem 275:19567-19576
15. Oliva JL, Griner EM, Kazanietz MG (2005) PKC isozymes and diacylglycerol-regulated proteins as effectors of growth factor receptors. Growth Factors 23:245-252
16. Corbalan-Garcia S, Gomez-Fernandez JC (2006) Protein kinase C regulatory domains: the art of decoding many different signals in membranes. Biochim Biophys Acta Mol Cell Biol Lipids 1761:633-654
17. Ono Y, Fujii T, Igarashi K, Kuno T, Tanaka C, Kikkawa U, Nishizuka Y (1989) Phorbol ester binding to protein kinase-C requires a cysteine-rich zinc-finger-like sequence. Proc Natl Acad Sci USA 86:4868-4871
18. Hurley JH, Newton AC, Parker PJ, Blumberg PM, Nishizuka Y (1997) Taxonomy and function of C1 protein kinase C homology domains. Protein Sci 6:477-480
19. Gomez-Fernandez JC, Torrecillas A, Corbalan-Garcia S (2004) Diacylglycerols as activators of protein kinase C (Review). Mol Membr Biol 21:339-349
20. 2+-binding domain. J Biol Chem 273:15879-15882
21. Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375-2390
22. Colon-Gonzalez F, Kazanietz MG (2006) C1 domains exposed: from diacylglycerol binding to protein-protein interactions. Biochim Biophys Acta 1761:827-837
23. Keenan C, Kelleher D (1998) Protein kinase C and the cytoskeleton. Cell Signal 10:225-232
24. Newton AC (1997) Regulation of protein kinase C. Curr Opin Cell Biol 9:161-167
25. Hirai T, Chida K (2003) Protein kinase Czeta (PKCzeta): activation mechanisms and cellular functions. J Biochem (Tokyo) 133:1-7
26. Ways DK, Cook PP, Webster C, Parker PJ (1992) Effect of phorbol esters on protein kinase-C-zeta. J Biol Chem 267:4799-4805
27. Nakanishi H, Brewer KA, Exton JH (1993) Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 268:13-16
28. Limatola C, Schaap D, Moolenaar WH, van Blitterswijk WJ (1994) Phosphatidic acid activation of protein kinase C-zeta overexpressed in COS cells: comparison with other protein kinase C isotypes and other acidic lipids. Biochem J 304(Pt 3):1001-1008
29. Muller G, Ayoub M, Storz P, Rennecke J, Fabbro D, Pfizenmaier K (1995) PKC zeta is a molecular switch in signal transduction of TNF-alpha, bifunctionally regulated by ceramide and arachidonic acid. EMBO J 14:1961-1969
30. Takenawa T, Itoh T (2001) Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim Biophys Acta 1533:190-206
31. Takenawa T, Itoh T (2006) Membrane targeting and remodeling through phosphoinositide-binding domains. IUBMB Life 58:296-303
32. Gusarova GA, Dada LA, Kelly AM, Brodie C, Witters LA, Chandel NS, Sznajder JI (2009) Alpha 1-AMP-activated protein kinase regulates hypoxia-induced Na, K-ATPase endocytosis via direct phosphorylation of PKC zeta. Mol Cell Biol 29:3455-3464
33. Kolsch V, Charest PG, Firtel RA (2008) The regulation of cell motility and chemotaxis by phospholipid signaling. J Cell Sci 121:551-559
34. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514
35. Etienne-Manneville S, Hall A (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489-498
36. Hung TJ, Kemphues KJ (1999) PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126:127-135
37. Izumi Y, Hirose T, Tamai Y, Hirai S, Nagashima Y, Fujimoto T, Tabuse Y, Kemphues KJ, Ohno S (1998) An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J Cell Biol 143:95-106
38. Joberty G, Petersen C, Gao L, Macara IG (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531-539
39. Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T (2000) A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2:540-547
40. Qiu RG, Abo A, Steven Martin G (2000) A human homolog of the C. elegans polarity determinant Par-6 links Rac and Cdc42 to PKCzeta signaling and cell transformation. Curr Biol 10:697-707
41. Luna-Ulloa LB, Hernandez-Maqueda JG, Castaneda-Patlan MC, Robles-Flores M (2011) Protein kinase C in Wnt signaling: implications in cancer initiation and progression. IUBMB Life 63:873-879
42. Schlessinger K, McManus EJ, Hall A (2007) Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J Cell Biol 178:355-361
43. Ishida-Takagishi M, Enomoto A, Asai N, Ushida K, Watanabe T, Hashimoto T, Kato T, Weng L, Matsumoto S, Asai M, Murakumo Y, Kaibuchi K, Kikuchi A, Takahashi M (2012) The Dishevelled-associating protein Daple controls the non-canonical Wnt/Rac pathway and cell motility. Nat Commun 3:859
44. Luna-Ulloa LB, Hernandez-Maqueda JG, Santoyo-Ramos P, Castaneda-Patlan MC, Robles-Flores M (2011) Protein kinase C zeta is a positive modulator of canonical Wnt signaling pathway in tumoral colon cell lines. Carcinogenesis 32:1615-1624
45. To C, Kulkarni S, Pawson T, Honda T, Gribble GW, Sporn MB, Wrana JL, Di Guglielmo GM (2008) The synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9- dien-28-oic acid-imidazolide alters transforming growth factor beta-dependent signaling and cell migration by affecting the cytoskeleton and the polarity complex. J Biol Chem 283:11700-11713
46. Frederick LA, Matthews JA, Jamieson L, Justilien V, Thompson EA, Radisky DC, Fields AP (2008) Matrix metalloproteinase-10 is a critical effector of protein kinase Ciota-Par6alpha-mediated lung cancer. Oncogene 27:4841-4853
47. Loitto VM, Huang C, Sigal YJ, Jacobson K (2007) Filopodia are induced by aquaporin-9 expression. Exp Cell Res 313:1295-1306
48. Laudanna C, Sorio C, Tecchio C, Butcher EC, Bonora A, Bassi C, Scarpa A (2003) Motility analysis of pancreatic adenocarcinoma cells reveals a role for the atypical zeta isoform of protein kinase C in cancer cell movement. Lab Invest 83:1155-1163
49. Palma-Nicolas JP, Lopez E, Lopez-Colome AM (2010) Thrombin stimulates RPE cell motility by PKC-zeta- and NF-kappaB-dependent gene expression of MCP-1 and CINC-1/GRO chemokines. J Cell Biochem 110:948-967
50. Kuribayashi K, Nakamura K, Tanaka M, Sato T, Kato J, Sasaki K, Takimoto R, Kogawa K, Terui T, Takayama T, Onuma T, Matsunaga T, Niitsu Y (2007) Essential role of protein kinase C zeta in transducing a motility signal induced by superoxide and a chemotactic peptide, fMLP. J Cell Biol 176:1049-1060
51. Sun R, Gao P, Chen L, Ma D, Wang J, Oppenheim JJ, Zhang N (2005) Protein kinase C zeta is required for epidermal growth factor-induced chemotaxis of human breast cancer cells. Cancer Res 65:1433-1441
52. Xiao A, Yin C, Yang C, Di Cristofano A, Pandolfi PP, Van Dyke T (2005) Somatic induction of Pten loss in a preclinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. Cancer Res 65:5172-5180
53. Powell CT, Fair WR, Heston WD (1994) Differential expression of protein kinase C isozyme messenger RNAs in dunning R-3327 rat prostatic tumors. Cell Growth Differ 5:143-149
54. Powell CT, Gschwend JE, Fair WR, Brittis NJ, Stec D, Huryk R (1996) Overexpression of protein kinase C-zeta (PKC-zeta) inhibits invasive and metastatic abilities of Dunning R-3327 MAT-LyLu rat prostate cancer cells. Cancer Res 56:4137-4141
55. Petit I, Goichberg P, Spiegel A, Peled A, Brodie C, Seger R, Nagler A, Alon R, Lapidot T (2005) Atypical PKC-zeta regulates SDF-1-mediated migration and development of human CD34+ progenitor cells. J Clin Invest 115:168-176
56. Forde S, Tye BJ, Newey SE, Roubelakis M, Smythe J, McGuckin CP, Pettengell R, Watt SM (2007) Endolyn (CD164) modulates the CXCL12-mediated migration of umbilical cord blood CD133+ cells. Blood 109:1825-1833
57. Guo H, Ma Y, Zhang B, Sun B, Niu R, Ying G, Zhang N (2009) Pivotal advance: PKCzeta is required for migration of macrophages. J Leukoc Biol 85:911-918
58. Gorshkova I, He D, Berdyshev E, Usatuyk P, Burns M, Kalari S, Zhao Y, Pendyala S, Garcia JG, Pyne NJ, Brindley DN, Natarajan V (2008) Protein kinase C-epsilon regulates sphingosine 1-phosphate-mediated migration of human lung endothelial cells through activation of phospholipase D2, protein kinase C-zeta, and Rac1. J Biol Chem 283:11794-11806
59. Crean JK, Furlong F, Finlay D, Mitchell D, Murphy M, Conway B, Brady HR, Godson C, Martin F (2004) Connective tissue growth factor [CTGF]/CCN2 stimulates mesangial cell migration through integrated dissolution of focal adhesion complexes and activation of cell polarization. FASEB J 18:1541-1543
60. Furlong F, Crean J, Thornton L, O'Leary R, Murphy M, Martin F (2007) Dysregulated intracellular signaling impairs CTGF-stimulated responses in human mesangial cells exposed to high extracellular glucose. Am J Physiol Renal Physiol 292:F1691-F1700
61. Buccione R, Orth JD, McNiven MA (2004) Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5:647-657
62. Linder S, Aepfelbacher M (2003) Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 13:376-385
63. Linder S (2007) The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 17:107-117
64. Collin O, Na S, Chowdhury F, Hong M, Shin ME, Wang F, Wang N (2008) Self-organized podosomes are dynamic mechanosensors. Curr Biol 18:1288-1294
65. Stylli SS, Kaye AH, Lock P (2008) Invadopodia: at the cutting edge of tumour invasion. J Clin Neurosci 15:725-737
66. Mueller SC, Chen WT (1991) Cellular invasion into matrix beads: localization of beta 1 integrins and fibronectin to the invadopodia. J Cell Sci 99(Pt 2):213-225
67. Baldassarre M, Pompeo A, Beznoussenko G, Castaldi C, Cortellino S, McNiven MA, Luini A, Buccione R (2003) Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol Biol Cell 14:1074-1084
68. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC (2006) Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 66:3034-3043
69. Xiao H, Li DX, Liu M (2012) Knowledge translation: airway epithelial cell migration and respiratory diseases. Cell Mol Life Sci. doi: 10.1007/s00018-012-1044-z
70. Xiao H, Eves R, Yeh C, Kan W, Xu F, Mak AS, Liu M (2009) Phorbol ester-induced podosomes in normal human bronchial epithelial cells. J Cell Physiol 218:366-375
71. Xiao H, Bai XH, Kapus A, Lu WY, Mak AS, Liu M (2010) The protein kinase C cascade regulates recruitment of matrix metalloprotease 9 to podosomes and its release and activation. Mol Cell Biol 30:5545-5561
72. Gatesman A, Walker VG, Baisden JM, Weed SA, Flynn DC (2004) Protein kinase Calpha activates c-Src and induces podosome formation via AFAP-110. Mol Cell Biol 24:7578-7597
73. Walker VG, Ammer A, Cao Z, Clump AC, Jiang BH, Kelley LC, Weed SA, Zot H, Flynn DC (2007) PI3 K activation is required for PMA-directed activation of cSrc by AFAP-110. Am J Physiol Cell Physiol 293:C119-C132
74. Dorfleutner A, Cho Y, Vincent D, Cunnick J, Lin H, Weed SA, Stehlik C, Flynn DC (2008) Phosphorylation of AFAP-110 affects podosome lifespan in A7r5 cells. J Cell Sci 121:2394-2405
75. Xiao H, Han B, Lodyga M, Bai XH, Wang Y, Liu M (2012) The actin-binding domain of actin filament-associated protein (AFAP) is involved in the regulation of cytoskeletal structure. Cell Mol Life Sci 69:1137-1151
76. Xiao H, Bai X-H, Wang Y, Kim H, Mak AS, Liu M (2012) MEK/ERK pathway mediates PKC activation-induced recruitment of PKC zeta and MMP-9 to podosomes. J Cell Physiol. doi: 10.1002/jcp.24146
77. Rodriguez EM, Dunham EE, Martin GS (2009) Atypical protein kinase C activity is required for extracellular matrix degradation and invasion by Src-transformed cells. J Cell Physiol 221:171-182
78. Urtreger AJ, Grossoni VC, Falbo KB, Kazanietz MG, Bal de Kier Joffe EM (2005) Atypical protein kinase C-zeta modulates clonogenicity, motility, and secretion of proteolytic enzymes in murine mammary cells. Mol Carcinog 42:29-39
79. Esteve PO, Chicoine E, Robledo O, Aoudjit F, Descoteaux A, Potworowski EF, St-Pierre Y (2002) Protein kinase C-zeta regulates transcription of the matrix metalloproteinase-9 gene induced by IL-1 and TNF-alpha in glioma cells via NF-kappa B. J Biol Chem 277:35150-35155
80. Huang HC, Huang CY, Lin-Shiau SY, Lin JK (2009) Ursolic acid inhibits IL-1beta or TNF-alpha-induced C6 glioma invasion through suppressing the association ZIP/p62 with PKC-zeta and downregulating the MMP-9 expression. Mol Carcinog 48:517-531
81. Roffey J, Rosse C, Linch M, Hibbert A, McDonald NQ, Parker PJ (2009) Protein kinase C intervention: the state of play. Curr Opin Cell Biol 21:268-279