Home LiteratureArticle Details
PMID: 19762474 Published · ppublish English Journal Article

Hypoxia-inducible factor-1-mediated regulation of semaphorin 4D affects tumor growth and vascularity.

The Journal of biological chemistry ·Vol. 284 ·No. 46 ·2009-11-13 ·Pages 32066-74

Sun Q, Zhou H, Binmadi NO, Basile JR

Abstract

Tumor progression and metastasis depend on the ability of cancer cells to initiate angiogenesis to ensure delivery of oxygen, nutrients, and growth factors to tumor cells and provide access to the systemic circulation. Hypoxia-inducible factor-1 (HIF-1) can activate expression of a broad range of genes that mediate many of the adaptive responses to decreased oxygen concentration, such as enhanced glucose uptake and formation of new blood vessels. Acting through Plexin-B1 on endothelial cells, Semaphorin 4D (Sema4D) has been shown to promote angiogenesis and enhance invasive growth and proliferation in some tumors. Here we show that the gene for Sema4D, the product of which is elevated in head and neck squamous cell carcinoma (HNSCC) cells, contains upstream hypoxia response elements (HRE) and is strongly induced in hypoxia in a HIF-1-dependent manner. Knocking down Sema4D expression with short hairpin (sh) RNA reduces in vitro endothelial cell migration and growth and vascularity of HNSCC xenografts expressing a degradation resistant HIF-1alpha subunit. We also demonstrate a correlation between HIF-1 activity and Sema4D expression in HNSCC specimens. These findings indicate that Sema4D is induced by hypoxia in a HIF-1-dependent manner and influences endothelial cell migration and tumor vascularity. Expression of Sema4D may be a strategy by which carcinomas promote angiogenesis and therefore could represent a therapeutic target for these malignancies.

MeSH Terms
Animals Antigens, CD/genetics,metabolism Blotting, Western Carcinoma, Squamous Cell/blood supply,metabolism,pathology Cell Hypoxia Cell Movement Cells, Cultured Chromatin Immunoprecipitation Endothelium, Vascular/cytology,metabolism Fluorescent Antibody Technique Gene Expression Regulation, Neoplastic Head and Neck Neoplasms/blood supply,metabolism,pathology Humans Hypoxia-Inducible Factor 1, alpha Subunit/genetics,metabolism Immunoenzyme Techniques Luciferases/metabolism Mice Mice, Nude Neovascularization, Pathologic RNA, Messenger/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction Semaphorins/genetics,metabolism Umbilical Veins/cytology,metabolism
Chemicals
Antigens, CD CD100 antigen HIF1A protein, human Hypoxia-Inducible Factor 1, alpha Subunit RNA, Messenger Semaphorins Luciferases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sun Qiangming
Department of Oncology and Diagnostic Sciences, University of Maryland Dental School, Baltimore, Maryland 21201, USA.
Zhou Hua
Binmadi Nada O
Basile John R
References (24)
24 references, click to expand
  1. Semaphorin-plexin signaling guides patterning of the developing vasculature.
    Dev Cell. 2004 Jul;7(1):117-23 PMID: 15239959
  2. Persistent activation of the Akt pathway in head and neck squamous cell carcinoma: a potential target for UCN-01.
    Clin Cancer Res. 2004 Jun 15;10(12 Pt 1):4029-37 PMID: 15217935
  3. Purification and characterization of hypoxia-inducible factor 1.
    J Biol Chem. 1995 Jan 20;270(3):1230-7 PMID: 7836384
  4. Role of neuropilins and semaphorins in angiogenesis and cancer.
    Ann Hematol. 2002;81 Suppl 2:S74 PMID: 12611086
  5. MT1-MMP controls tumor-induced angiogenesis through the release of semaphorin 4D.
    J Biol Chem. 2007 Mar 2;282(9):6899-905 PMID: 17204469
  6. High-resolution structure of the catalytic region of MICAL (molecule interacting with CasL), a multidomain flavoenzyme-signaling molecule.
    Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16836-41 PMID: 16275925
  7. Transcriptional regulation by p53: one protein, many possibilities.
    Cell Death Differ. 2006 Jun;13(6):951-61 PMID: 16575405
  8. Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexin-B.
    Cancer Res. 2004 Aug 1;64(15):5212-24 PMID: 15289326
  9. Common mechanisms of nerve and blood vessel wiring.
    Nature. 2005 Jul 14;436(7048):193-200 PMID: 16015319
  10. Hypoxia-inducible factor-1 (HIF-1).
    Mol Pharmacol. 2006 Nov;70(5):1469-80 PMID: 16887934
  11. Computational detection and location of transcription start sites in mammalian genomic DNA.
    Genome Res. 2002 Mar;12(3):458-61 PMID: 11875034
  12. Regulation of angiogenesis by hypoxia-inducible factor 1.
    Crit Rev Oncol Hematol. 2006 Jul;59(1):15-26 PMID: 16716598
  13. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1.
    Mol Cell Biol. 1996 Sep;16(9):4604-13 PMID: 8756616
  14. Controlling the immune system through semaphorins.
    Sci STKE. 2002 Apr 16;2002(128):re4 PMID: 11972358
  15. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein.
    EMBO J. 2000 Aug 15;19(16):4298-309 PMID: 10944113
  16. Met-HGF/SF: tumorigenesis, invasion and metastasis.
    Ciba Found Symp. 1997;212:119-30; discussion 130-2, 148-54 PMID: 9524767
  17. CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes.
    Blood. 2003 Mar 1;101(5):1962-9 PMID: 12406905
  18. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis.
    Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9017-22 PMID: 16754882
  19. Plexin-B1 plays a redundant role during mouse development and in tumour angiogenesis.
    BMC Dev Biol. 2007 May 22;7:55 PMID: 17519029
  20. Unified nomenclature for the semaphorins/collapsins. Semaphorin Nomenclature Committee.
    Cell. 1999 May 28;97(5):551-2 PMID: 10367884
  21. Microtumor growth initiates angiogenic sprouting with simultaneous expression of VEGF, VEGF receptor-2, and angiopoietin-2.
    J Clin Invest. 2002 Mar;109(6):777-85 PMID: 11901186
  22. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha.
    Genes Dev. 1998 Jan 15;12(2):149-62 PMID: 9436976
  23. Prognostic significance of CD100 expression in soft tissue sarcoma.
    Cancer. 2007 Jul 1;110(1):164-72 PMID: 17520683
  24. Semaphorin 4D/plexin-B1 induces endothelial cell migration through the activation of PYK2, Src, and the phosphatidylinositol 3-kinase-Akt pathway.
    Mol Cell Biol. 2005 Aug;25(16):6889-98 PMID: 16055703
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2009-11-13
Epub
2009-00-17
Pages
32066-74
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2797277
Subset
IM
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: [email protected]