Home LiteratureArticle Details
PMID: 23135917 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

RhoB differentially controls Akt function in tumor cells and stromal endothelial cells during breast tumorigenesis.

Cancer research ·Vol. 73 ·No. 1 ·2013-01-01 ·Pages 50-61

Kazerounian S, Gerald D, Huang M, Chin YR, Udayakumar D, Zheng N, O'Donnell RK, Perruzzi C, Mangiante L, Pourat J, Phung TL, Bravo-Nuevo A, Shechter S, McNamara S, Duhadaway JB, Kocher ON, Brown LF, Toker A, Prendergast GC, Benjamin LE

Abstract

Tumors are composed of cancer cells but also a larger number of diverse stromal cells in the tumor microenvironment. Stromal cells provide essential supports to tumor pathophysiology but the distinct characteristics of their signaling networks are not usually considered in developing drugs to target tumors. This oversight potentially confounds proof-of-concept studies and increases drug development risks. Here, we show in established murine and human models of breast cancer how differential regulation of Akt by the small GTPase RhoB in cancer cells or stromal endothelial cells determines their dormancy versus outgrowth when angiogenesis becomes critical. In cancer cells in vitro or in vivo, RhoB functions as a tumor suppressor that restricts EGF receptor (EGFR) cell surface occupancy as well as Akt signaling. However, after activation of the angiogenic switch, RhoB functions as a tumor promoter by sustaining endothelial Akt signaling, growth, and survival of stromal endothelial cells that mediate tumor neoangiogenesis. Altogether, the positive impact of RhoB on angiogenesis and progression supercedes its negative impact in cancer cells themselves. Our findings elucidate the dominant positive role of RhoB in cancer. More generally, they illustrate how differential gene function effects on signaling pathways in the tumor stromal component can complicate the challenge of developing therapeutics to target cancer pathophysiology.

MeSH Terms
Animals Breast Neoplasms/metabolism,pathology Carcinoma, Ductal, Breast/metabolism,pathology Cell Transformation, Neoplastic/metabolism Endothelial Cells/metabolism Female Flow Cytometry Gene Expression Regulation, Neoplastic Humans Immunoblotting Immunohistochemistry Immunoprecipitation In Situ Hybridization Mice Mice, Transgenic Neovascularization, Pathologic/metabolism Proto-Oncogene Proteins c-akt/metabolism Real-Time Polymerase Chain Reaction Stromal Cells/metabolism Tumor Microenvironment/physiology rhoB GTP-Binding Protein/metabolism
Chemicals
Proto-Oncogene Proteins c-akt rhoB GTP-Binding Protein
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Kazerounian Shiva
Department of Pathology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, USA.
Gerald Damien
Huang Minzhou
Chin Y Rebecca
Udayakumar Durga
Zheng Ningning
O'Donnell Rebekah K
Perruzzi Carole
Mangiante Lee
Pourat Jacob
Phung Thuy L
Bravo-Nuevo Arturo
Shechter Sharon
McNamara Stephanie
Duhadaway James B
Kocher Olivier N
Brown Lawrence F
Toker Alex
Prendergast George C
Benjamin Laura E
References (43)
43 references, click to expand
  1. RhoB is required to mediate apoptosis in neoplastically transformed cells after DNA damage.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6192-7 PMID: 11353846
  2. Nobiletin, a citrus flavonoid, suppresses invasion and migration involving FAK/PI3K/Akt and small GTPase signals in human gastric adenocarcinoma AGS cells.
    Mol Cell Biochem. 2011 Jan;347(1-2):103-15 PMID: 20963626
  3. RhoB controls Akt trafficking and stage-specific survival of endothelial cells during vascular development.
    Genes Dev. 2003 Nov 1;17(21):2721-32 PMID: 14597666
  4. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis.
    Cell. 1996 Aug 9;86(3):353-64 PMID: 8756718
  5. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures.
    Methods. 2003 Jul;30(3):256-68 PMID: 12798140
  6. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo.
    Cell. 1987 May 22;49(4):465-75 PMID: 3032456
  7. Farnesyl transferase inhibitors induce apoptosis of Ras-transformed cells denied substratum attachment.
    Cancer Res. 1997 Feb 15;57(4):708-13 PMID: 9044849
  8. Transcriptional activation of the small GTPase gene rhoB by genotoxic stress is regulated via a CCAAT element.
    Nucleic Acids Res. 2001 Feb 1;29(3):792-8 PMID: 11160903
  9. Both farnesylated and geranylgeranylated RhoB inhibit malignant transformation and suppress human tumor growth in nude mice.
    J Biol Chem. 2000 Jun 16;275(24):17974-8 PMID: 10770919
  10. Expression profiles frame the promoter specificity dilemma of the ETS family of transcription factors.
    Nucleic Acids Res. 2004 Oct 21;32(18):5693-702 PMID: 15498926
  11. Selection of appropriate control genes to assess expression of tumor antigens using real-time RT-PCR.
    Biotechniques. 2004 Jan;36(1):84-6, 88, 90-1 PMID: 14740490
  12. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding.
    J Cell Biol. 2001 Jan 8;152(1):111-26 PMID: 11149925
  13. Activation of RhoB by hypoxia controls hypoxia-inducible factor-1alpha stabilization through glycogen synthase kinase-3 in U87 glioblastoma cells.
    Cancer Res. 2006 Jan 1;66(1):482-9 PMID: 16397264
  14. Friends or foes - bipolar effects of the tumour stroma in cancer.
    Nat Rev Cancer. 2004 Nov;4(11):839-49 PMID: 15516957
  15. Epigenetic regulation of RhoB loss of expression in lung cancer.
    BMC Cancer. 2007 Nov 30;7:220 PMID: 18047684
  16. Tumor-host interactions: a far-reaching relationship.
    J Clin Oncol. 2010 Sep 10;28(26):4022-8 PMID: 20644094
  17. Regulation of epidermal growth factor receptor traffic by the small GTPase rhoB.
    Curr Biol. 1999 Sep 9;9(17):955-8 PMID: 10508588
  18. Five novel hormone-responsive cell lines derived from murine mammary ductal carcinomas: in vivo and in vitro effects of estrogens and progestins.
    Cancer Res. 2001 Jan 1;61(1):293-302 PMID: 11196177
  19. A distinct role of RhoB in gastric cancer suppression.
    Int J Cancer. 2011 Mar 1;128(5):1057-68 PMID: 20473933
  20. Stromal fibroblasts in cancer initiation and progression.
    Nature. 2004 Nov 18;432(7015):332-7 PMID: 15549095
  21. Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases.
    FEBS Lett. 2001 Feb 16;490(3):142-52 PMID: 11223029
  22. In vivo restoration of RhoB expression leads to ovarian tumor regression.
    Cancer Gene Ther. 2008 Jul;15(7):456-64 PMID: 18340357
  23. The membrane targeting and spatial activation of Src, Yes and Fyn is influenced by palmitoylation and distinct RhoB/RhoD endosome requirements.
    J Cell Sci. 2007 Aug 1;120(Pt 15):2555-64 PMID: 17623777
  24. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis.
    BMC Cancer. 2007 Mar 27;7:55 PMID: 17389037
  25. Hallmarks of cancer: interactions with the tumor stroma.
    Exp Cell Res. 2010 May 1;316(8):1324-31 PMID: 20211171
  26. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells.
    Mol Cell Biol. 2001 Oct;21(20):6906-12 PMID: 11564874
  27. An integrative genomic and proteomic analysis of PIK3CA, PTEN, and AKT mutations in breast cancer.
    Cancer Res. 2008 Aug 1;68(15):6084-91 PMID: 18676830
  28. Loss of RhoB expression promotes migration and invasion of human bronchial cells via activation of AKT1.
    Cancer Res. 2009 Aug 1;69(15):6092-9 PMID: 19602596
  29. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat.
    J Cell Biol. 1989 Aug;109(2):903-14 PMID: 2760116
  30. Geranylgeranylated RhoB is sufficient to mediate tissue-specific suppression of Akt kinase activity by farnesyltransferase inhibitors.
    FEBS Lett. 2000 Sep 22;481(3):205-8 PMID: 11007964
  31. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini.
    Nat Cell Biol. 2001 Sep;3(9):785-92 PMID: 11533657
  32. Actin' up: RhoB in cancer and apoptosis.
    Nat Rev Cancer. 2001 Nov;1(2):162-8 PMID: 11905808
  33. Regulation of endocytic traffic by rho family GTPases.
    Trends Cell Biol. 2000 Mar;10(3):85-8 PMID: 10675900
  34. Loss of RhoB expression in human lung cancer progression.
    Clin Cancer Res. 2004 Apr 15;10(8):2742-50 PMID: 15102679
  35. Cloning of the human RHOB gene promoter: characterization of a VNTR sequence that affects transcriptional activity.
    Genomics. 2003 May;81(5):525-30 PMID: 12706111
  36. RhoB in cancer suppression.
    Histol Histopathol. 2006 Feb;21(2):213-8 PMID: 16329046
  37. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease.
    Mol Cell Biol. 1992 Mar;12(3):954-61 PMID: 1312220
  38. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility.
    Exp Cell Res. 2004 Nov 15;301(1):43-9 PMID: 15501444
  39. RhoB regulates PDGFR-beta trafficking and signaling in vascular smooth muscle cells.
    Arterioscler Thromb Vasc Biol. 2007 Dec;27(12):2597-605 PMID: 17951322
  40. Suppression of rho B expression in invasive carcinoma from head and neck cancer patients.
    Clin Cancer Res. 2002 Jul;8(7):2225-32 PMID: 12114424
  41. The L6 protein TM4SF1 is critical for endothelial cell function and tumor angiogenesis.
    Cancer Res. 2009 Apr 15;69(8):3272-7 PMID: 19351819
  42. RhoB loss prevents streptozotocin-induced diabetes and ameliorates diabetic complications in mice.
    Am J Pathol. 2011 Jan;178(1):245-52 PMID: 21224061
  43. RhoB is frequently downregulated in non-small-cell lung cancer and resides in the 2p24 homozygous deletion region of a lung cancer cell line.
    Int J Cancer. 2007 Feb 1;120(3):543-51 PMID: 17096327
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2013-01-01
Epub
2012-00-07
Pages
50-61
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC4201498
Subset
IM
Grants
NHLBI NIH HHS · R01 HL071049 · United States
NCI NIH HHS · K99 CA157945 · United States
NCI NIH HHS · K99CA157945 · United States
NCI NIH HHS · R01 CA100123 · United States
NIDDK NIH HHS · P30 DK034854 · United States
NCI NIH HHS · R01 CA109086 · United States
NCI NIH HHS · CA082222 · United States
NCI NIH HHS · CA0109086 · United States
NCI NIH HHS · P01 CA092644 · United States
NCI NIH HHS · R01 CA082222 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com