Abstract
Semaphorins are a large class of secreted or membrane-associated proteins that act as chemotactic cues for cell movement via their transmembrane receptors, plexins. We hypothesized that the function of the semaphorin signaling pathway in the control of cell migration could be harnessed by cancer cells during invasion and metastasis. We now report 13 somatic missense mutations in the cytoplasmic domain of the Plexin-B1 gene. Mutations were found in 89% (8 of 9) of prostate cancer bone metastases, in 41% (7 of 17) of lymph node metastases, and in 46% (41 of 89) of primary cancers. Forty percent of prostate cancers contained the same mutation. Overexpression of the Plexin-B1 protein was found in the majority of primary tumors. The mutations hinder Rac and R-Ras binding and R-RasGAP activity, resulting in an increase in cell motility, invasion, adhesion, and lamellipodia extension. These results identify a key role for Plexin-B1 and the semaphorin signaling pathway it mediates in prostate cancer.
MeSH Terms
Adenocarcinoma/genetics,pathology,secondary
Bone Neoplasms/genetics,secondary
Cell Adhesion/genetics
Cell Line, Tumor
Cell Movement/genetics
Gene Expression Regulation, Neoplastic
Humans
Lymphatic Metastasis/genetics
Male
Mutation, Missense
Neoplasm Invasiveness/genetics
Neoplasm Proteins/biosynthesis,genetics,physiology
Nerve Tissue Proteins/biosynthesis,genetics,physiology
Polymorphism, Single-Stranded Conformational
Prostatic Neoplasms/genetics,pathology
Protein Structure, Tertiary
Pseudopodia/ultrastructure
Receptors, Cell Surface/biosynthesis,genetics,physiology
Signal Transduction
rac1 GTP-Binding Protein/metabolism
ras Proteins/metabolism
Chemicals
Neoplasm Proteins
Nerve Tissue Proteins
PLXNB1 protein, human
RAC1 protein, human
Receptors, Cell Surface
RRAS protein, human
rac1 GTP-Binding Protein
ras Proteins
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Wong Oscar Gee-Wan
Prostate Cancer Research Centre, Institute of Urology, University College London, 67 Riding House Street, London W1W 7EJ, United Kingdom.
Nitkunan Tharani
Oinuma Izumi
Zhou Chun
Blanc Veronique
Brown Richard S D
Bott Simon R J
Nariculam Joseph
Box Gary
Munson Phillipa
Constantinou Jason
Feneley Mark R
Klocker Helmut
Eccles Suzanne A
Negishi Manabu
Freeman Alex
Masters John R
Williamson Magali
References (31)
31 references, click to expand
-
Structure of the semaphorin-3A receptor binding module.
Neuron. 2003 Aug 14;39(4):589-98
PMID: 12925274
-
Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons.
J Neurosci. 2004 Dec 15;24(50):11473-80
PMID: 15601954
-
Plexin signaling hampers integrin-based adhesion, leading to Rho-kinase independent cell rounding, and inhibiting lamellipodia extension and cell motility.
FASEB J. 2004 Mar;18(3):592-4
PMID: 14734633
-
Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology.
Neuron. 2002 Jul 3;35(1):51-63
PMID: 12123608
-
Semaphorins command cells to move.
Nat Rev Mol Cell Biol. 2005 Oct;6(10):789-800
PMID: 16314868
-
The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules.
Cell. 1993 Dec 31;75(7):1389-99
PMID: 8269517
-
Hepatocyte growth factor and its receptor (c-MET) in prostatic carcinoma.
Am J Pathol. 1995 Aug;147(2):386-96
PMID: 7639332
-
A family of transmembrane proteins with homology to the MET-hepatocyte growth factor receptor.
Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):674-8
PMID: 8570614
-
Scatter-factor and semaphorin receptors: cell signalling for invasive growth.
Nat Rev Cancer. 2002 Apr;2(4):289-300
PMID: 12001990
-
Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function.
Nature. 2003 Jul 24;424(6947):391-7
PMID: 12879061
-
Diversity of TMPRSS2-ERG fusion transcripts in the human prostate.
Oncogene. 2007 Apr 19;26(18):2667-73
PMID: 17043636
-
The spectrum of TP53 mutations in bladder carcinoma.
Genes Chromosomes Cancer. 1994 Feb;9(2):108-18
PMID: 7513540
-
Biological functions and signaling of a transmembrane semaphorin, CD100/Sema4D.
Cell Mol Life Sci. 2004 Feb;61(3):292-300
PMID: 14770294
-
Semaphorin 4D/Plexin-B1-mediated R-Ras GAP activity inhibits cell migration by regulating beta(1) integrin activity.
J Cell Biol. 2006 May 22;173(4):601-13
PMID: 16702230
-
Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions.
Development. 1999 May;126(10):2181-9
PMID: 10207143
-
The semaphorin 4D receptor controls invasive growth by coupling with Met.
Nat Cell Biol. 2002 Sep;4(9):720-4
PMID: 12198496
-
High expression of the Met receptor in prostate cancer metastasis to bone.
Urology. 2002 Dec;60(6):1113-7
PMID: 12475693
-
KLF6, a candidate tumor suppressor gene mutated in prostate cancer.
Science. 2001 Dec 21;294(5551):2563-6
PMID: 11752579
-
Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors.
Cell. 1999 Oct 1;99(1):59-69
PMID: 10520994
-
The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner.
Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12457-62
PMID: 11035813
-
Plexin-B1/RhoGEF-mediated RhoA activation involves the receptor tyrosine kinase ErbB-2.
J Cell Biol. 2004 Jun 21;165(6):869-80
PMID: 15210733
-
Mutations of the BRAF gene in human cancer.
Nature. 2002 Jun 27;417(6892):949-54
PMID: 12068308
-
Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates.
Cell. 1999 Oct 1;99(1):71-80
PMID: 10520995
-
The plexin-B1/Rac interaction inhibits PAK activation and enhances Sema4D ligand binding.
Genes Dev. 2002 Apr 1;16(7):836-45
PMID: 11937491
-
Androgen receptor mutations in prostate cancer.
Cancer Res. 2000 Feb 15;60(4):944-9
PMID: 10706109
-
Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database.
Hum Mutat. 2007 Jun;28(6):622-9
PMID: 17311302
-
Transcription factor E2F3 overexpressed in prostate cancer independently predicts clinical outcome.
Oncogene. 2004 Aug 5;23(35):5871-9
PMID: 15184867
-
Direct interaction of Rnd1 with Plexin-B1 regulates PDZ-RhoGEF-mediated Rho activation by Plexin-B1 and induces cell contraction in COS-7 cells.
J Biol Chem. 2003 Jul 11;278(28):25671-7
PMID: 12730235
-
The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras.
Science. 2004 Aug 6;305(5685):862-5
PMID: 15297673
-
ras oncogenes in human cancer: a review.
Cancer Res. 1989 Sep 1;49(17):4682-9
PMID: 2547513
-
Met, metastasis, motility and more.
Nat Rev Mol Cell Biol. 2003 Dec;4(12):915-25
PMID: 14685170