Atypical protein kinase C induces cell transformation by disrupting Hippo/Yap signaling

Molecular Biology of the Cell

Volumn 26, Issue 20, 2015, Pages 3578-3595

  Archibald, Andrew ^a,b   Al Masri, Maia ^a,b   Liew Spilger, Alyson ^a   McCaffrey, Luke ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMOT PROTEIN; CASPASE 3; GREEN FLUORESCENT PROTEIN; PROTEIN; PROTEIN KINASE C; PROTEIN MST1; PROTEIN MST2; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; UVOMORULIN; AMOT PROTEIN, HUMAN; HIPPO PROTEIN, HUMAN; ISOPROTEIN; LATS1 PROTEIN, HUMAN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; PKC-3 PROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER GRADING; CELL DISRUPTION; CELL JUNCTION; CELL POLARITY; CELL PROLIFERATION; CELL SHAPE; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTACT INHIBITION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; GENE SILENCING; GROWTH REGULATION; HIPPOCAMPUS; HUMAN; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANIMAL; DOG; HEK293 CELL LINE; MDCK CELL LINE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL POLARITY; CELL TRANSFORMATION, NEOPLASTIC; CONTACT INHIBITION; DOGS; EPITHELIAL CELLS; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84944104862     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-05-0265     Document Type: Article

References (75)

1. Adler JJ, Johnson DE, Heller BL, Bringman LR, Ranahan WP, Conwell MD, Sun Y, Hudmon A, Wells CD (2013). Serum deprivation inhibits the transcriptional co-Activator YAP and cell growth via phosphorylation of the 130-kDa isoform of Angiomotin by the LATS1/2 protein kinases. Proc Natl Acad Sci USA 110, 17368-17373.
2. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, Dupont S, Piccolo S (2013). A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059.
3. Aranda V, Haire T, Nolan ME, Calarco JP, Rosenberg AZ, Fawcett JP, Pawson T, Muthuswamy SK (2006). Par6-APKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat Cell Biol 8, 1235-1245.
4. Atwood SX, Li M, Lee A, Tang JY, Oro AE (2013). GLI activation by atypical protein kinase C iota/lambda regulates the growth of basal cell carcinomas. Nature 494, 484-488.
5. Avruch J, Zhou D, Fitamant J, Bardeesy N, Mou F, Barrufet LR (2012). Protein kinases of the Hippo pathway: regulation and substrates. Semin Cell Dev Biol 23, 770-784.
6. Bryant DM, Datta A, Rodriguez-Fraticelli AE, Peranen J, Martin-Belmonte F, Mostov KE (2010). A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12, 1035-1045.
7. Cao X, Pfaff SL, Gage FH (2008). YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev 22, 3320-3334.
8. Cerruti B, Puliafito A, Shewan AM, Yu W, Combes AN, Little MH, Chianale F, Primo L, Serini G, Mostov KE, et al. (2013). Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures. J Cell Biol 203, 359-372.
9. Chan EH, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HH (2005). The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24, 2076-2086.
10. Chan SW, Lim CJ, Guo F, Tan I, Leung T, Hong W (2013). Actin-binding and cell proliferation activities of angiomotin family members are regulated by Hippo pathway-mediated phosphorylation. J Biol Chem 288, 37296-37307.
11. Chen Q, Zhang N, Gray RS, Li H, Ewald AJ, Zahnow CA, Pan D (2014). A temporal requirement for Hippo signaling in mammary gland differentiation, growth, and tumorigenesis. Genes Dev 28, 432-437.
12. Chou MM, Hou W, Johnson J, Graham LK, Lee MH, Chen CS, Newton AC, Schaffhausen BS, Toker A (1998). Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr Biol 8, 1069-1077.
13. Cohen EE, Lingen MW, Zhu B, Zhu H, Straza MW, Pierce C, Martin LE, Rosner MR (2006). Protein kinase C zeta mediates epidermal growth factor-induced growth of head and neck tumor cells by regulating mitogen-Activated protein kinase. Cancer Res 66, 6296-6303.
14. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti Anna R, Poletti A, et al. (2011). The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147, 759-772.
15. Desai S, Pillai P, Win-Piazza H, Acevedo-Duncan M (2011). PKC-iota promotes glioblastoma cell survival by phosphorylating and inhibiting BAD through a phosphatidylinositol 3-kinase pathway. Biochim Biophys Acta 1813, 1190-1197.
16. Du GS, Wang JM, Lu JX, Li Q, Ma CQ, Du JT, Zou SQ (2009). Expression of P-APKC-iota, E-cadherin, and beta-catenin related to invasion and metastasis in hepatocellular carcinoma. Ann Surg Oncol 16, 1578-1586.
17. Durgan J, Kaji N, Jin D, Hall A (2011). Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J Biol Chem 286, 12461-12474.
18. Eder AM, Sui X, Rosen DG, Nolden LK, Cheng KW, Lahad JP, Kango-Singh M, Lu KH, Warneke CL, Atkinson EN, et al. (2005). Atypical PKCiota contributes to poor prognosis through loss of apical-basal polarity and cyclin E overexpression in ovarian cancer. Proc Natl Acad Sci USA 102, 12519-12524.
19. Eisenhoffer GT, Rosenblatt J (2013). Bringing balance by force: live cell extrusion controls epithelial cell numbers. Trends Cell Biol 23, 185-192.
20. Evans JD, Cornford PA, Dodson A, Neoptolemos JP, Foster CS (2003). Expression patterns of protein kinase C isoenzymes are characteristically modulated in chronic pancreatitis and pancreatic cancer. Am J Clin Pathol 119, 392-402.
21. Ferrari A, Veligodskiy A, Berge U, Lucas MS, Kroschewski R (2008). ROCKmediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation. J Cell Sci 121, 3649-3663.
22. Fields AP, Frederick LA, Regala RP (2007). Targeting the oncogenic protein kinase Ciota signalling pathway for the treatment of cancer. Biochem Soc Trans 35, 996-1000.
23. Genevet A, Tapon N (2011). The Hippo pathway and apico-basal cell polarity. Biochem J 436, 213-224.
24. Glantschnig H, Rodan GA, Reszka AA (2002). Mapping of MST1 kinase sites of phosphorylation. Activation and autophosphorylation. J Biol Chem 277, 42987-42996.
25. Graybill C, Wee B, Atwood SX, Prehoda KE (2012). Partitioning-defective protein 6 (Par-6) activates atypical protein kinase C (aPKC) by pseudosubstrate displacement. J Biol Chem 287, 21003-21011.
26. Grifoni D, Garoia F, Bellosta P, Parisi F, De Biase D, Collina G, Strand D, Cavicchi S, Pession A (2007). aPKCzeta cortical loading is associated with Lgl cytoplasmic release and tumor growth in Drosophila and human epithelia. Oncogene 26, 5960-5965.
27. Grzeschik NA, Parsons LM, Allott ML, Harvey KF, Richardson HE (2010). Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr Biol 20, 573-581.
28. Halaoui R, McCaffrey L (2014). Rewiring cell polarity signaling in cancer. Oncogene 34, 939-950.
29. Hao Y, Du Q, Chen X, Zheng Z, Balsbaugh JL, Maitra S, Shabanowitz J, Hunt DF, Macara IG (2010). Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical pins. Curr Biol 20, 1809-1818.
30. Hogan C, Dupre-Crochet S, Norman M, Kajita M, Zimmermann C, Pelling AE, Piddini E, Baena-Lopez LA, Vincent JP, Itoh Y, et al. (2009). Characterization of the interface between normal and transformed epithelial cells. Nat Cell Biol 11, 460-467.
31. Iden S, van Riel Wilhelmina E, Scher R, Song J-Y, Hirose T, Ohno S, Collard John G (2012). Tumor type-dependent function of the Par3 polarity protein in skin tumorigenesis. Cancer Cell 22, 389-403.
32. Jaffe AB, Kaji N, Durgan J, Hall A (2008). Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J Cell Biol 183, 625-633.
33. Justilien V, Fields AP (2009). Ect2 links the PKCiota-Par6alpha complex to Rac1 activation and cellular transformation. Oncogene 28, 3597-3607.
34. Justilien V, Walsh MP, Ali SA, Thompson EA, Murray NR, Fields AP (2014). The PRKCI and SOX2 oncogenes are coamplified and cooperate to activate Hedgehog signaling in lung squamous cell carcinoma. Cancer Cell 25, 139-151.
35. Kadono Y, Okada Y, Namiki M, Seiki M, Sato H (1998). Transformation of epithelial Madin-Darby canine kidney cells with p60(v-src) induces expression of membrane-Type 1 matrix metalloproteinase and invasiveness. Cancer Res 58, 2240-2244.
36. Kato S, Akimoto K, Nagashima Y, Ishiguro H, Kubota K, Kobayashi N, Hosono K, Watanabe S, Sekino Y, Sato T, et al. (2013). aPKClambda/iota is a beneficial prognostic marker for pancreatic neoplasms. Pancreatology 13, 360-368.
37. Kojima Y, Akimoto K, Nagashima Y, Ishiguro H, Shirai S, Chishima T, Ichikawa Y, Ishikawa T, Sasaki T, Kubota Y, et al. (2008). The overexpression and altered localization of the atypical protein kinase C lambda/iota in breast cancer correlates with the pathologic type of these tumors. Hum Pathol 39, 824-831. 63.
38. Langzam L, Koren R, Gal R, Kugel V, Paz A, Farkas A, Sampson SR (2001). Patterns of protein kinase C isoenzyme expression in transitional cell carcinoma of bladder. Relation to degree of malignancy. Am J Clin Pathol 116, 377-385.
39. Levchenko T, Bratt A, Arbiser JL, Holmgren L (2004). Angiomotin expression promotes hemangioendothelioma invasion. Oncogene 23, 1469-1473.
40. Lin YM, Su CC, Su WW, Hwang JM, Hsu HH, Tsai CH, Wang YC, Tsai FJ, Huang CY, Liu JY, Chen LM (2012). Expression of protein kinase C isoforms in cancerous breast tissue and adjacent normal breast tissue. Chin J Physiol 55, 55-61.
41. Linch M, Sanz-Garcia M, Rosse C, Riou P, Peel N, Madsen CD, Sahai E, Downward J, Khwaja A, Dillon C, et al. (2014). Regulation of polarized morphogenesis by protein kinase C iota in oncogenic epithelial spheroids. Carcinogenesis 35, 396-406.
42. Ma Y, Yang Y, Wang F, Wei Q, Qin H (2014). Hippo-YAP signaling pathway: a new paradigm for cancer therapy. Int J Cancer 2014, doi: 10.1002/ijc.29073.
43. Martin-Belmonte F, Perez-Moreno M (2011). Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer 12, 23-38.
44. McCaffrey Luke M, Montalbano J, Mihai C, Ian Macara G (2012). Loss of the Par3 polarity protein promotes breast tumorigenesis and metastasis. Cancer Cell 22, 601-614.
45. Moleirinho S, Guerrant W, Kissil JL (2014). The angiomotins-from discovery to function. FEBS Lett 588, 2693-2703.
46. Namdarian B, Wong E, Galea R, Pedersen J, Chin X, Speirs R, Humbert PO, Costello AJ, Corcoran NM, Hovens CM (2013). Loss of APKC expression independently predicts tumor recurrence in superficial bladder cancers. Urol Oncol 31, 649-655.
47. Nishimura T, Kaibuchi K (2007). Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13, 15-28.
48. Paget JA, Restall IJ, Daneshmand M, Mersereau JA, Simard MA, Parolin D AE, Lavictoire SJ, Amin MS, Islam S, Lorimer IAJ (2011). Repression of cancer cell senescence by PKC. Oncogene 31, 3584-3596.
49. Paramasivam M, Sarkeshik A, Yates JR 3rd, Fernandes MJ, McCollum D (2011). Angiomotin family proteins are novel activators of the LATS2 kinase tumor suppressor. Mol Biol Cell 22, 3725-3733.
50. Paul A, Gunewardena S, Stecklein SR, Saha B, Parelkar N, Danley M, Rajendran G, Home P, Ray S, Jokar I, et al. (2014). PKClambda/iota signaling promotes triple-negative breast cancer growth and metastasis. Cell Death Differ 21, 1469-1481.
51. Piccolo S, Dupont S, Cordenonsi M (2014). The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev 94, 1287-1312.
52. Pu YS, Huang CY, Chen JY, Kang WY, Lin YC, Shiu YS, Chuang SJ, Yu HJ, Lai MK, Tsai YC, et al. (2012). Down-regulation of PKCzeta in renal cell carcinoma and its clinicopathological implications. J Biomed Sci 19, 39.
53. Puliafito A, Hufnagel L, Neveu P, Streichan S, Sigal A, Fygenson DK, Shraiman BI (2012). Collective and single cell behavior in epithelial contact inhibition. Proc Natl Acad Sci USA 109, 739-744.
54. Regala RP, Weems C, Jamieson L, Khoor A, Edell ES, Lohse CM, Fields AP (2005). Atypical protein kinase C iota is an oncogene in human nonsmall cell lung cancer. Cancer Res 65, 8905-8911.
55. Romano D, Matallanas D, Frederick DT, Flaherty KT, Kolch W (2014). One Hippo and many masters: differential regulation of the Hippo pathway in cancer. Biochem Soc Trans 42, 816-821.
56. Sakurai A, Matsuda M, Kiyokawa E (2012). Activated Ras protein accelerates cell cycle progression to perturb Madin-Darby canine kidney cystogenesis. J Biol Chem 287, 31703-31711.
57. Sanz L, Sanchez P, Lallena MJ, Diaz-Meco MT, Moscat J (1999). The interaction of p62 with RIP links the atypical PKCs to NF-kappaB activation. EMBO J 18, 3044-3053.
58. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, Camargo FD (2011). Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144, 782-795.
59. Smith CA, Lau KM, Rahmani Z, Dho SE, Brothers G, She YM, Berry DM, Bonneil E, Thibault P, Schweisguth F, et al. (2007). aPKC-mediated phosphorylation regulates asymmetric membrane localization of the cell fate determinant Numb. EMBO J 26, 468-480.
60. Sotillos S, Diaz-Meco MT, Caminero E, Moscat J, Campuzano S (2004). DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J Cell Biol 166, 549-557.
61. Standaert ML, Bandyopadhyay G, Perez L, Price D, Galloway L, Poklepovic A, Sajan MP, Cenni V, Sirri A, Moscat J, et al. (1999). Insulin activates protein kinases C-zeta and C-lambda by an autophosphorylationdependent mechanism and stimulates their translocation to GLUT4 vesicles and other membrane fractions in rat adipocytes. J Biol Chem 274, 25308-25316.
62. Toyli M, Rosberg-Kulha L, Capra J, Vuoristo J, Eskelinen S (2010). Different responses in transformation of MDCK cells in 2D and 3D culture by v-Src as revealed by microarray techniques, RT-PCR and functional assays. Lab Invest 90, 915-928.
63. Tsai JH, Hsieh YS, Kuo SJ, Chen ST, Yu SY, Huang CY, Chang AC, Wang YW, Tsai MT, Liu JY (2000). Alteration in the expression of protein kinase C isoforms in human hepatocellular carcinoma. Cancer Lett 161, 171-175.
64. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL (2010). The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 19, 831-844.
65. Varelas X, Wrana JL (2012). Coordinating developmental signaling: novel roles for the Hippo pathway. Trends Cell Biol 22, 88-96.
66. Yang CC, Graves HK, Moya IM, Tao C, Hamaratoglu F, Gladden AB, Halder G (2015). Differential regulation of the Hippo pathway by adherens junctions and apical-basal cell polarity modules. Proc Natl Acad Sci USA 112, 1785-1790.
67. Yang YL, Chu JY, Luo ML, Wu YP, Zhang Y, Feng YB, Shi ZZ, Xu X, Han YL, Cai Y, et al. (2008). Amplification of PRKCI, located in 3q26, is associated with lymph node metastasis in esophageal squamous cell carcinoma. Genes Chromosomes Cancer 47, 127-136.
68. Yao S, Bee A, Brewer D, Dodson A, Beesley C, Ke Y, Ambroisine L, Fisher G, Moller H, Dickinson T, et al. (2010). PRKC-zeta expression promotes the aggressive phenotype of human prostate cancer cells and is a novel target for therapeutic intervention. Genes Cancer 1, 444-464.
69. Yao S, Ireland SJ, Bee A, Beesley C, Forootan SS, Dodson A, Dickinson T, Gerard P, Lian LY, Risk JM, et al. (2012). Splice variant PRKC-zeta(-PrC) is a novel biomarker of human prostate cancer. Br J Cancer 107, 388-399.
70. Yi C, Shen Z, Stemmer-Rachamimov A, Dawany N, Troutman S, Showe LC, Liu Q, Shimono A, Sudol M, Holmgren L, et al. (2013). The p130 isoform of angiomotin is required for Yap-mediated hepatic epithelial cell proliferation and tumorigenesis. Sci Signal 6, ra77.
71. Yin F, Yu J, Zheng Y, Chen Q, Zhang N, Pan D (2013). Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 154, 1342-1355.
72. Yin J, Liu Z, Li H, Sun J, Chang X, Liu J, He S, Li B (2014). Association of PKCzeta expression with clinicopathological characteristics of breast cancer. PLoS One 9, e90811.
73. Yu FX, Guan KL (2013). The Hippo pathway: regulators and regulations. Genes Dev 27, 355-371.
74. Zhang H, Liu G, Dziubinski M, Yang Z, Ethier SP, Wu G (2008). Comprehensive analysis of oncogenic effects of PIK3CA mutations in human mammary epithelial cells. Breast Cancer Res Treat 112, 217-227.
75. Zhao B, Li L, Lu Q, Wang LH, Liu CY, Lei Q, Guan KL (2011). Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev 25, 51-63.