The G12 family proteins upregulate matrix metalloproteinase-2 via p53 leading to human breast cell invasion

Breast Cancer Research and Treatment

Volumn 124, Issue 1, 2010, Pages 49-61

  Kim, Eun Sook ^a   Jeong, Jae Boon ^a   Kim, Seonhoe ^a   Lee, Kyung Min ^b   Ko, Eunyoung ^b   Noh, Dong Young ^b   Hwang, Ki Tae ^c   Ha, Ji Hee ^d   Lee, Chang Ho ^e   Kim, Sang Geon ^c   Moon, Aree ^a  

^a Duksung Women's University   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c Seoul National University   (South Korea)

^d University of Odlahoma   (United States)

^e Hanyang University   (South Korea)

Author keywords

Breast cell invasion; G 12 13; MMP 2; p53

Indexed keywords

GELATINASE A; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN 12; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA 12; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA 13; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; PROTEIN KINASE B; PROTEIN P53; RAC1 PROTEIN; RAS PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MAP2K3 PROTEIN, HUMAN; MAP2K6 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE P38; MMP2 PROTEIN, HUMAN; RAC1 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BREAST CANCER; CANCER CELL; CANCER INVASION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN SYNTHESIS; TRANSCRIPTION INITIATION; UPREGULATION; ADULT; AGED; BREAST TUMOR; CELL MOTION; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; GENOTYPE; METABOLISM; MIDDLE AGED; MUTATION; PAGET NIPPLE DISEASE; PATHOLOGY; TUMOR CELL LINE;

ADULT; AGED; AGED, 80 AND OVER; BINDING SITES; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOTYPE; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HUMANS; MAP KINASE KINASE 3; MAP KINASE KINASE 6; MATRIX METALLOPROTEINASE 2; MIDDLE AGED; MUTATION; NEOPLASM INVASIVENESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RAC1 GTP-BINDING PROTEIN; RAS PROTEINS; TRANSCRIPTION, GENETIC; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 77957709002     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-009-0697-2     Document Type: Article

References (51)

1. N Dhanasekaran JM Dermott 1996 Signaling by the G12 class of G proteins Cell Signal 8 235 245 1:CAS:528:DyaK28XkvFKhsrc%3D 10.1016/0898-6568(96)00048-4 8842523
2. K Yoshioka F Matsumura H Akedo K Itoh 1998 Small GTP-binding protein Rho stimulates the actomyosin system, leading to invasion of tumor cells J Biol Chem 273 5146 5154 1:CAS:528:DyaK1cXhs1Cnt7w%3D 10.1074/jbc.273.9.5146 9478968
3. C Huang KM Hujer Z Wu RT Miller 2004 The Ca2 + -sensing receptor couples to Galpha12/13 to activate phospholipase D in Madin-Darby canine kidney cells Am J Physiol Cell Physiol 286 C22 C30 1:CAS:528:DC%2BD2cXot1WhsQ%3D%3D 10.1152/ajpcell.00229.2003 12954603
4. U Rumenapp M Asmus H Schablowski M Woznicki L Han KH Jakobs M Fahimi-Vahid C Michalek T Wieland M Schmidt 2001 The M3 muscarinic acetylcholine receptor expressed in HEK-293 cells signals to phospholipase D via G12 but not Gq-type G proteins: regulators of G proteins as tools to dissect pertussis toxin-resistant G proteins in receptor-effector coupling J Biol Chem 276 2474 2479 1:CAS:528:DC%2BD3MXhtVGjs7o%3D 10.1074/jbc.M004957200 11036069
5. LW Shepard M Yang P Xie DD Browning T Voyno-Yasenetskaya T Kozasa RD Ye 2001 Constitutive activation of NF-kappa B and secretion of interleukin-8 induced by the G protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus involve G alpha(13) and RhoA J Biol Chem 276 45979 45987 1:CAS:528:DC%2BD3MXptVymsLs%3D 10.1074/jbc.M104783200 11590141
6. S Fukuhara MJ Marinissen M Chiariello JS Gutkind 2000 Signaling from G protein-coupled receptors to ERK5/Big MAPK 1 involves Galpha q and Galpha 12/13 families of heterotrimeric G proteins. Evidence for the existence of a novel Ras AND Rho-independent pathway J Biol Chem 275 21730 21736 1:CAS:528: DC%2BD3cXkvFGit78%3D 10.1074/jbc.M002410200 10781600
7. M Nishida S Tanabe Y Maruyama S Mangmool K Urayama Y Nagamatsu S Takagahara JH Turner T Kozasa H Kobayashi Y Sato T Kawanishi R Inoue T Nagao H Kurose 2005 G alpha 12/13- and reactive oxygen species-dependent activation of c-Jun NH2-terminal kinase and p38 mitogen-activated protein kinase by angiotensin receptor stimulation in rat neonatal cardiomyocytes J Biol Chem 280 18434 18441 1:CAS:528:DC%2BD2MXjsl2htLY%3D 10.1074/jbc.M409710200 15743761
8. H Mitsui N Takuwa K Kurokawa JH Exton Y Takuwa 1997 Dependence of activated Galpha12-induced G1 to S phase cell cycle progression on both Ras/mitogen-activated protein kinase and Ras/Rac1/Jun N-terminal kinase cascades in NIH3T3 fibroblasts J Biol Chem 272 4904 4910 1:CAS:528:DyaK2sXhsValtL8%3D 10.1074/jbc.272.8.4904 9030549
9. N Xu L Bradley I Ambdukar JS Gutkind 1993 A mutant alpha subunit of G12 potentiates the eicosanoid pathway and is highly oncogenic in NIH 3T3 cells Proc Natl Acad Sci USA 90 6741 6745 1:CAS:528:DyaK3sXmtVSkt7k%3D 10.1073/pnas.90.14.6741 8393576
10. MV Vara Prasad SK Shore N Dhanasekaran 1994 Activated mutant of G alpha 13 induces Egr-1, c-fos, and transformation in NIH 3T3 cells Oncogene 9 2425 2429 1:STN:280:DyaK2czgvF2hsw%3D%3D 8036026
11. TE Meigs TA Fields DD McKee PJ Casey 2001 Interaction of Galpha 12 and Galpha 13 with the cytoplasmic domain of cadherin provides a mechanism for beta -catenin release Proc Natl Acad Sci USA 98 519 524 1:CAS:528: DC%2BD3MXnslKhtQ%3D%3D 10.1073/pnas.021350998 11136230
12. P Kelly PJ Casey TE Meigs 2007 Biologic functions of the G12 subfamily of heterotrimeric g proteins: growth, migration, and metastasis Biochemistry 46 6677 6687 1:CAS:528:DC%2BD2sXlt1OgsrY%3D 10.1021/bi700235f 17503779
13. D Bian C Mahanivong J Yu SM Frisch ZK Pan RD Ye S Huang 2006 The G12/13-RhoA signaling pathway contributes to efficient lysophosphatidic acid-stimulated cell migration Oncogene 25 2234 2244 1:CAS:528: DC%2BD28XjtFOqsr0%3D 10.1038/sj.onc.1209261 16301993
14. P Kelly LN Stemmle JF Madden TA Fields Y Daaka PJ Casey 2006 A role for the G12 family of heterotrimeric G proteins in prostate cancer invasion J Biol Chem 281 26483 26490 1:CAS:528:DC%2BD28XovFyqu78%3D 10.1074/jbc.M604376200 16787920
15. P Kelly BJ Moeller J Juneja MA Booden CJ Der Y Daaka MW Dewhirst TA Fields PJ Casey 2006 The G12 family of heterotrimeric G proteins promotes breast cancer invasion and metastasis Proc Natl Acad Sci USA 103 8173 8178 1:CAS:528:DC%2BD28Xlt1Ohur8%3D 10.1073/pnas.0510254103 16705036
16. WG Stetler-Stevenson 1999 Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention J Clin Invest 103 1237 1241 1:CAS:528:DyaK1MXivFansrk%3D 10.1172/JCI6870 10225966
17. A Moon MS Kim TG Kim SH Kim HE Kim YQ Chen HR Kim 2000 H-ras, but not N-ras, induces an invasive phenotype in human breast epithelial cells: a role for MMP-2 in the H-ras-induced invasive phenotype Int J Cancer 85 176 181 1:CAS:528:DC%2BD3cXmsVCjuw%3D%3D 10629074
18. MS Kim EJ Lee HR Kim A Moon 2003 p38 kinase is a key signaling molecule for H-Ras-induced cell motility and invasive phenotype in human breast epithelial cells Cancer Res 63 5454 5461 1:CAS:528:DC%2BD3sXntleku7o%3D 14500381
19. H Qin Y Sun EN Benveniste 1999 The transcription factors Sp1, Sp3, and AP-2 are required for constitutive matrix metalloproteinase-2 gene expression in astroglioma cells J Biol Chem 274 29130 29137 1:CAS:528:DyaK1MXmslWqt7g%3D 10.1074/jbc.274.41.29130 10506168
20. J Bian Y Sun 1997 Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase 2) promoter Mol Cell Biol 17 6330 6338 1:CAS:528:DyaK2sXntVSjt74%3D 9343394
21. MR Bergman S Cheng N Honbo L Piacentini JS Karliner DH Lovett 2003 A functional activating protein 1 (AP-1) site regulates matrix metalloproteinase 2 (MMP-2) transcription by cardiac cells through interactions with JunB-Fra1 and JunB-FosB heterodimers Biochem J 369 485 496 1:CAS:528:DC%2BD3sXit1aqurs%3D 10.1042/BJ20020707 12371906
22. H Song SH Ki SG Kim A Moon 2006 Activating transcription factor 2 mediates matrix metalloproteinase-2 transcriptional activation induced by p38 in breast epithelial cells Cancer Res 66 10487 10496 1:CAS:528:DC%2BD28XhtFGjsrbP 10.1158/0008-5472.CAN-06-1461 17079470
23. HD Soule TM Maloney SR Wolman WD Peterson Jr.R.Brenz CM McGrath J Russo RJ Pauley RF Jones SC Brooks 1990 Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10 Cancer Res 50 6075 6086 1:CAS:528:DyaK3MXktFSq 1975513
24. M Abdellatif WR MacLellan MD Schneider 1994 p21 Ras as a governor of global gene expression J Biol Chem 69 15423 15426
25. SI Han SY Oh SH Woo KH Kim JH Kim HD Kim HS Kang 2001 Implication of a small GTPase Rac1 in the activation of c-Jun N-terminal kinase and heat shock factor in response to heat shock J Biol Chem 276 1889 1895 1:CAS:528: DC%2BD3MXotVChsQ%3D%3D 10.1074/jbc.M006042200 11050083
26. Z Ma H Qin EN Benveniste 2001 Transcriptional suppression of matrix metalloproteinase-9 gene expression by IFN-gamma and IFN-beta: critical role of STAT-1alpha J Immunol 167 5150 5159 1:CAS:528:DC%2BD3MXotVWjsL4%3D 11673527
27. MS Kim SM Lee WD Kim SH Ki A Moon CH Lee SG Kim 2007 G alpha 12/13 basally regulates p53 through Mdm4 expression Mol Cancer Res 5 473 484 1:CAS:528:DC%2BD2sXmtVOisrw%3D 10.1158/1541-7786.MCR-06-0395 17510313
28. F Sabeh I Ota K Holmbeck H Birkedal-Hansen P Soloway M Balbin C Lopez-Otin S Shapiro M Inada S Krane E Allen D Chung SJ Weiss 2004 Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP J Cell Biol 167 769 781 1:CAS:528:DC%2BD2cXhtVaqtb3J 10.1083/jcb.200408028 15557125
29. SH Ki IJ Cho DW Choi SG Kim 2005 Glucocorticoid receptor (GR)-associated SMRT binding to C/EBPbeta TAD and Nrf2 Neh4/5: role of SMRT recruited to GR in GSTA2 gene repression Mol Cell Biol 25 4150 4165 1:CAS:528:DC%2BD2MXktlSmu7c%3D 10.1128/MCB.25.10.4150-4165.2005 15870285
30. A Moon H-Y Yong J-I Song D Cukovic S Salagrama D Kaplan D Putt H Kim A Dombkowski HR Kim 2008 Global gene expression profiling unveils S100A8/A9 as candidate markers in H-ras-mediated human breast epithelial cell invasion Mol Cancer Res 6 1544 1553 1:CAS:528:DC%2BD1cXht1Cmsb7I 10.1158/1541-7786.MCR-08- 0189 18922970
31. R Kaunas P Nguyen S Usami S Chien 2005 Cooperative effects of Rho and mechanical stretch on stress fiber organization PNAS 102 15895 15900 1:CAS:528:DC%2BD2MXht1Wru7bF 10.1073/pnas.0506041102 16247009
32. VM Braga LM Machesky A Hall NA Hotchin 1997 The Small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts J Cell Biol 137 1421 1431 1:CAS:528:DyaK2sXjvF2msr8%3D 10.1083/jcb.137.6.1421 9182672
33. CD Nobes A Hall 1999 Rho GTPases control polarity, protrusion, and adhesion during cell movement J Cell Biol 144 1235 1244 1:CAS:528: DyaK1MXitVKjtbo%3D 10.1083/jcb.144.6.1235 10087266
34. UM Munoz-Najar KM Neurath F Vumbaca KP Claffey 2006 Hypoxia stimulates breast carcinoma cell invasion through MT1-MMP and MMP-2 activation Oncogene 25 2379 2392 1:CAS:528:DC%2BD28XjsVWrsrw%3D 10.1038/sj.onc.1209273 16369494
35. K Ghosh CK Thodeti AC Dudley A Mammoto M Klagsbrun DE Ingber 2008 Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro PNAS 105 11305 11310 1:CAS:528: DC%2BD1cXhtVShu7zM 10.1073/pnas.0800835105 18685096
36. EA Goncharova DA Goncharov PN Lim D Noonan VP Krymskaya 2006 Modulation of cell migration and invasiveness by tumor suppressor TSC2 in lymphangioleiomyomatosis Am J Respir Cell Mol Biol 34 473 480 1:CAS:528:DC%2BD28XjsFCqu7o%3D 10.1165/rcmb.2005-0374OC 16388022
37. I Shin S Kim H Song HR Kim A Moon 2005 H-Ras-specific activation of Rac-MKK3/6-p38 pathway: its critical role in invasion and migration of breast epithelial cells J Biol Chem 280 14675 14683 1:CAS:528:DC%2BD2MXjtFSmurY%3D 10.1074/jbc.M411625200 15677464
38. A Jemal R Siegel E Ward T Murray J Xu MJ Thun 2007 Cancer statistics, 2007 CA Cancer J Clin 57 43 66 10.3322/canjclin.57.1.43 17237035
39. D Lepley JH Paik T Hla F Ferrer 2005 The G protein-coupled receptor S1P2 regulates Rho/Rho kinase pathway to inhibit tumor cell migration Cancer Res 5 3788 3795 10.1158/0008-5472.CAN-04-2311
40. HA Chapman 1997 Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration Curr Opin Cell Biol 9 714 724 1:CAS:528:DyaK2sXmsFCgsbc%3D 10.1016/S0955-0674(97)80126-3 9330876
41. R Chirco XW Liu KK Jung HR Kim 2006 Novel functions of TIMPs in cell signaling Cancer Metastasis Rev 25 99 113 1:CAS:528:DC%2BD28Xktlaksro%3D 10.1007/s10555-006-7893-x 16680576
42. R Haffner M Oren 1995 Biochemical properties and biological effects of p53 Curr Opin Genet Dev 5 84 90 1:CAS:528:DyaK2MXjvFegsbs%3D 10.1016/S0959-437X(95)90058-6 7749331
43. LJ Ko C Prives 1997 p53: puzzle and paradigm Genes Dev 10 1054 1072 10.1101/gad.10.9.1054
44. SJ Wadsworth G Gebauer GD van Rossum N Dhanasekaran 1997 Ras-dependent signaling by the GTPase-deficient mutant of Galpha12 J Biol Chem 272 28829 28832 1:CAS:528:DyaK2sXnsVKks7Y%3D 10.1074/jbc.272.46.28829 9360946
45. LR Collins A Minden M Karin JH Brown 1996 Galpha12 stimulates c-Jun NH2-terminal kinase through the small G proteins Ras and Rac J Biol Chem 271 17349 17353 1:CAS:528:DyaK28XksFamtLg%3D 10.1074/jbc.271.29.17349 8663428
46. JM Dermott JH Ha CH Lee N Dhanasekaran 2004 Differential regulation of Jun N-terminal kinase and p38MAP kinase by Galpha12 Oncogene 23 226 232 1:CAS:528:DC%2BD2cXovVKgsA%3D%3D 10.1038/sj.onc.1207009 14712227
47. M Nagao Y Kaziro H Itoh 1999 The Src family tyrosine kinase is involved in Rho-dependent activation of c-Jun N-terminal kinase by Galpha12 Oncogene 18 4425 4434 1:CAS:528:DyaK1MXlsVOksL4%3D 10.1038/sj.onc.1202832 10442633
48. EH Jho RJ Davis CC Malbon 1997 c-Jun amino-terminal kinase is regulated by Ga12/Ga13 and obligate for differentiation of P19 embryonal carcinoma cells by retinoic acid J Biol Chem 272 24468 24474 1:CAS:528:DyaK2sXmsFamsb0%3D 10.1074/jbc.272.39.24468 9305908
49. H Kurose 2003 Ga12 and Ga13 as key regulatory mediator in signal transduction Life Sci 74 155 161 1:CAS:528:DC%2BD3sXos12qtrs%3D 10.1016/j.lfs.2003.09.003 14607242
50. YV Berestetskaya MP Faure H Ichijo TA Voyno-Yasenetskaya 1998 Regulation of apoptosis by α-subunits of G12 and G13 proteins via apoptosis signal-regulating kinase-1 J Biol Chem 273 27816 27823 1:CAS:528: DyaK1cXntVCmt78%3D 10.1074/jbc.273.43.27816 9774391
51. YV Berestetskaya MP Faure H Ichijo TA Voyno-Yasenetskaya 2001 Interaction between the Gα subunit of heterotrimeric G12 protein and Hsp90 is required for Gα12 signaling J Biol Chem 276 46088 46093 10.1074/jbc.M108711200