Protein kinase Cδ is required for ErbB2-driven mammary gland tumorigenesis and negatively correlates with prognosis in human breast cancer

Oncogene

Volumn 33, Issue 10, 2014, Pages 1306-1315

  Allen Petersen, B L ^a   Carter, C J ^b   Ohm, A M ^b   Reyland, M E ^b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

ErbB2; PKC breast cancer; Src

Indexed keywords

CASPASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR 2; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C DELTA; SHORT HAIRPIN RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; BREAST CANCER; BREAST CARCINOGENESIS; BREAST TUMOR; CANCER CELL; CANCER PROGNOSIS; CELL COUNT; COMPARATIVE STUDY; CONTROLLED STUDY; DENSITOMETRY; DIMERIZATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MAMMARY GLAND; MOUSE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECURRENCE FREE SURVIVAL; SIGNAL TRANSDUCTION;

MOUSE MAMMARY TUMOR VIRUS; MUS; MUS MUSCULUS;

ANIMALS; BREAST NEOPLASMS; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, KNOCKOUT; PROGNOSIS; PROTEIN KINASE C-DELTA; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION;

EID: 84895924663     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.59     Document Type: Article

References (61)

1. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235: 177-182
2. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244: 707-712
3. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997; 16: 1647-1655
4. Jones JT, Akita RW, Sliwkowski MX. Binding specificities and affinities of egf domains for ErbB receptors. FEBS Lett 1999; 447: 227-231
5. Reyland ME. Protein kinase C isoforms: Multi-functional regulators of cell life and death. Front Biosci 2009; 14: 2386-2399
6. Dempsey EC, Newton AC, Mochly-Rosen D, Fields AP, Reyland ME, Insel PA et al. Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol 2000; 279: L429-L438
7. Newton AC. Protein kinase C: Structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev 2001; 101: 2353-2364
8. DeVries TA, Neville MC, Reyland ME. Nuclear import of PKCdelta is required for apoptosis: Identification of a novel nuclear import sequence. Embo J 2002; 21: 6050-6060
9. DeVries-Seimon TA, Ohm AM, Humphries MJ, Reyland ME. Induction of apoptosis is driven by nuclear retention of protein kinase C delta. J Biol Chem 2007; 282: 22307-22314
10. Matassa AA, Carpenter L, Biden TJ, Humphries MJ, Reyland ME. PKCdelta is required for mitochondrial-dependent apoptosis in salivary epithelial cells. J Biol Chem 2001; 276: 29719-29728
11. Reyland ME, Anderson SM, Matassa AA, Barzen KA, Quissell DO. Protein kinase C delta is essential for etoposide-induced apoptosis in salivary gland acinar cells. J Biol Chem 1999; 274: 19115-19123
12. Humphries MJ, Limesand KH, Schneider JC, Nakayama KI, Anderson SM, Reyland ME. Suppression of apoptosis in the protein kinase Cdelta null mouse in vivo. J Biol Chem 2006; 281: 9728-9737
13. Allen-Petersen BL, Miller MR, Neville MC, Anderson SM, Nakayama KI, Reyland ME. Loss of protein kinase C delta alters mammary gland development and apoptosis. Cell Death Dis 2010; 1: E17
14. McKiernan E, O'Brien K, Grebenchtchikov N, Geurts-Moespot A, Sieuwerts AM, Martens JW et al. Protein kinase Cdelta expression in breast cancer as measured by real-time PCR, western blotting and ELISA. Br J Cancer 2008; 99: 1644-1650
15. Evans JD, Cornford PA, Dodson A, Neoptolemos JP, Foster CS. Expression patterns of protein kinase C isoenzymes are characteristically modulated in chronic pancreatitis and pancreatic cancer. Am J Clin Pathol 2003; 119: 392-402
16. Pongracz J, Clark P, Neoptolemos JP, Lord JM. Expression of protein kinase C isoenzymes in colorectal cancer tissue and their differential activation by different bile acids. Int J Cancer 1995; 61: 35-39
17. D'Costa AM, Robinson JK, Maududi T, Chaturvedi V, Nickoloff BJ, Denning MF. The proapoptotic tumor suppressor protein kinase C-delta is lost in human squamous cell carcinomas. Oncogene 2006; 25: 378-386
18. Varga A, Czifra G, Tallai B, Nemeth T, Kovacs I, Kovacs L et al. Tumor gradedependent alterations in the protein kinase C isoform pattern in urinary bladder carcinomas. Eur Urol 2004; 46: 462-465
19. Symonds JM, Ohm AM, Carter CJ, Heasley LE, Boyle TA, Franklin WA et al. Protein kinase C delta is a downstream effector of oncogenic K-ras in lung tumors. Cancer Res 2011; 71: 2087-2097
20. Keshamouni VG, Mattingly RR, Reddy KB. Mechanism of 17-beta-estradiol- induced Erk1/2 activation in breast cancer cells. A role for HER2 AND PKC-delta. J Biol Chem 2002; 277: 22558-22565
21. Iwabu A, Smith K, Allen FD, Lauffenburger DA, Wells A. Epidermal growth factor induces fibroblast contractility and motility via a protein kinase C delta-dependent pathway. J Biol Chem 2004; 279: 14551-14560
22. Kiley SC, Clark KJ, Duddy SK, Welch DR, Jaken S. Increased protein kinase C delta in mammary tumor cells: Relationship to transformtion and metastatic progression. Oncogene 1999; 18: 6748-6757
23. Kiley SC, Clark KJ, Goodnough M, Welch DR, Jaken S. Protein kinase C delta involvement in mammary tumor cell metastasis. Cancer Res 1999; 59: 3230-3238
24. Kruger JS, Reddy KB. Distinct mechanisms mediate the initial and sustained phases of cell migration in epidermal growth factor receptor-overexpressing cells. Mol Cancer Res 2003; 1: 801-809
25. Zhang S, Huang WC, Li P, Guo H, Poh SB, Brady SW et al. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat Med 2011; 17: 461-469
26. Rexer BN, Ham AJ, Rinehart C, Hill S, Granja-Ingram Nde M, Gonzalez-Angulo AM et al. Phosphoproteomic mass spectrometry profiling links Src family kinases to escape from HER2 tyrosine kinase inhibition. Oncogene 2011; 30: 4163-4174
27. Song JS, Swann PG, Szallasi Z, Blank U, Blumberg PM, Rivera J. Tyrosine phosphorylation-dependent and -independent associations of protein kinase C-delta with Src family kinases in the RBL-2H3 mast cell line: Regulation of Src family kinase activity by protein kinase C-delta. Oncogene 1998; 16: 3357-3368
28. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. ONCOMINE: A cancer microarray database and integrated data-mining platform. Neoplasia 2004; 6: 1-6
29. Ringner M, Fredlund E, Hakkinen J, Borg A, Staaf J. GOBO: Gene expression-based outcome for breast cancer online. PLoS One 2011; 6: E17911
30. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009; 27: 1160-1167
31. Bouchard L, Lamarre L, Tremblay PJ, Jolicoeur P. Stochastic appearance of mammary tumors in transgenic mice carrying the MMTV/c-neu oncogene. Cell 1989; 57: 931-936
32. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci USA 1992; 89: 10578-10582
33. Muthuswamy SK, Gilman M, Brugge JS. Controlled dimerization of ErbB receptors provides evidence for differential signaling by homo- and heterodimers. Mol Cell Biol 1999; 19: 6845-6857
34. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001; 3: 785-792
35. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 2005; 5: 675-688
36. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003; 30: 256-268
37. Kwon YK, Bhattacharyya A, Alberta JA, Giannobile WV, Cheon K, Stiles CD et al. Activation of ErbB2 during wallerian Degeneration of sciatic nerve. J Neurosci 1997; 17: 8293-8299
38. Dankort DL, Wang Z, Blackmore V, Moran MF, Muller WJ. Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation. Mol Cell Biol 1997; 17: 5410-5425
39. Dankort D, Jeyabalan N, Jones N, Dumont DJ, Muller WJ. Multiple ErbB-2/Neu phosphorylation sites mediate transformation through distinct effector proteins. J Biol Chem 2001; 276: 38921-38928
40. Xu W, Yuan X, Beebe K, Xiang Z, Neckers L. Loss of Hsp90 association up-regulates Src-dependent ErbB2 activity. Mol Cell Biol 2007; 27: 220-228
41. Menard S, Tagliabue E, Campiglio M, Pupa SM. Role of HER2 gene overexpression in breast carcinoma. J Cell Physiol 2000; 182: 150-162
42. Marmor MD, Skaria KB, Yarden Y. Signal transduction and oncogenesis by ErbB/ HER receptors. Int J Radiat Oncol Biol Phys 2004; 58: 903-913
43. Zhou X, Agazie YM. Molecular mechanism for SHP2 in promoting HER2-induced signaling and transformation. J Biol Chem 2009; 284: 12226-12234
44. Dankort D, Maslikowski B, Warner N, Kanno N, Kim H, Wang Z et al. Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB-2)-induced mammary tumorigenesis: Implications for human breast cancer. Mol Cell Biol 2001; 21: 1540-1551
45. Schade B, Lam SH, Cernea D, Sanguin-Gendreau V, Cardiff RD, Jung BL et al. Distinct ErbB-2 coupled signaling pathways promote mammary tumors with unique pathologic and transcriptional profiles. Cancer Res 2007; 67: 7579-7588
46. Marcotte R, Zhou L, Kim H, Roskelly CD, Muller WJ. c-Src associates with ErbB2 through an interaction between catalytic domains and confers enhanced transforming potential. Mol Cell Biol 2009; 29: 5858-5871
47. Muthuswamy SK, Siegel PM, Dankort DL, Webster MA, Muller WJ. Mammary tumors expressing the neu proto-oncogene possess elevated c-Src tyrosine kinase activity. Mol Cell Biol 1994; 14: 735-743
48. Tan M, Li P, Klos KS, Lu J, Lan KH, Nagata Y et al. ErbB2 promotes Src synthesis and stability: Novel mechanisms of Src activation that confer breast cancer metastasis. Cancer Res 2005; 65: 1858-1867
49. Cheng J, Watkins SC, Walker WH. Testosterone activates mitogen-activated protein kinase via Src kinase and the epidermal growth factor receptor in sertoli cells. Endocrinology 2007; 148: 2066-2074
50. Kraus S, Benard O, Naor Z, Seger R. c-Src is activated by the epidermal growth factor receptor in a pathway that mediates JNK and ERK activation by gonadotropin-releasing hormone in COS7 cells. J Biol Chem 2003; 278: 32618-32630
51. Liu D, Lu JS, Yin XL. [Role of pp60c-src in mitogen-activated protein kinase activation of vascular smooth muscle cells]. Sheng Li Xue Bao 2000; 52: 483-486
52. Zhang HT, O'Rourke DM, Zhao H, Murali R, Mikami Y, Davis JG et al. Absence of autophosphorylation site Y882 in the p185neu oncogene product correlates with a reduction of transforming potential. Oncogene 1998; 16: 2835-2842
53. Jackson D, Zheng Y, Lyo D, Shen Y, Nakayama K, Nakayama KI et al. Suppression of cell migration by protein kinase Cdelta. Oncogene 2005; 24: 3067-3072
54. Lu Z, Hornia A, Jiang YW, Zang Q, Ohno S, Foster DA. Tumor promotion by depleting cells of protein kinase C delta. Mol Cell Biol 1997; 17: 3418-3428
55. Miyamoto A, Nakayama K, Imaki H, Hirose S, Jiang Y, Abe M et al. Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cdelta. Nature 2002; 416: 865-869
56. Grossoni VC, Falbo KB, Kazanietz MG, de Kier Joffe ED, Urtreger AJ. Protein kinase C delta enhances proliferation and survival of murine mammary cells. Mol Carcinog 2007; 46: 381-390
57. Mauro LV, Grossoni VC, Urtreger AJ, Yang C, Colombo LL, Morandi A et al. PKC Delta (PKCdelta) promotes tumoral progression of human Ductal pancreatic cancer. Pancreas 2010; 39: E31-e41
58. Ma XJ, Salunga R, Tuggle JT, Gaudet J, Enright E, McQuary P et al. Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA 2003; 100: 5974-5979
59. Perou CM, Sorlie T, Eisen MB, van De Rijn M, Jeffrey SS, Rees CA et al. Molecular portraits of human breast tumours. Nature 2000; 406: 747-752
60. Tolwinski NS, Shapiro PS, Goueli S, Ahn NG. Nuclear localization of mitogenactivated protein kinase kinase 1 (MKK1) is promoted by serum stimulation and G2-M progression. Requirement for phosphorylation at the activation lip and signaling downstream of MKK. J Biol Chem 1999; 274: 6168-6174
61. Adwan TS, Ohm AM, Jones DN, Humphries MJ, Reyland ME. Regulated binding of importin-alpha to protein kinase Cdelta in response to apoptotic signals facilitates nuclear import. J Biol Chem 2011; 286: 35716-35724