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PMID: 18451146 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization.

Cancer research ·Vol. 68 ·No. 9 ·2008-05-01 ·Pages 3204-13

Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma C, Kazarov AR, Andzelm MM, Strominger JL, Brown M, Hemler ME

Abstract

CD151, a master regulator of laminin-binding integrins (alpha(6)beta(4), alpha(6)beta(1), and alpha(3)beta(1)), assembles these integrins into complexes called tetraspanin-enriched microdomains. CD151 protein expression is elevated in 31% of human breast cancers and is even more elevated in high-grade (40%) and estrogen receptor-negative (45%) subtypes. The latter includes triple-negative (estrogen receptor, progesterone receptor, and HER2 negative) basal-like tumors. CD151 ablation markedly reduced basal-like mammary cell migration, invasion, spreading, and signaling (through FAK, Rac1, and lck) while disrupting epidermal growth factor receptor (EGFR)-alpha(6) integrin collaboration. Underlying these defects, CD151 ablation redistributed alpha(6)beta(4) integrins subcellularly and severed molecular links between integrins and tetraspanin-enriched microdomains. In a prototypical basal-like mammary tumor line, CD151 ablation notably delayed tumor progression in ectopic and orthotopic xenograft models. These results (a) establish that CD151-alpha(6) integrin complexes play a functional role in basal-like mammary tumor progression; (b) emphasize that alpha(6) integrins function via CD151 linkage in the context of tetraspanin-enriched microdomains; and (c) point to potential relevance of CD151 as a high-priority therapeutic target, with relative selectivity (compared with laminin-binding integrins) for pathologic rather than normal physiology.

MeSH Terms
Animals Antigens, CD/genetics,metabolism,physiology Breast Neoplasms/genetics,metabolism,pathology Cell Adhesion/genetics Cell Movement/genetics Disease Progression Epidermal Growth Factor/pharmacology Gene Expression Regulation, Neoplastic Humans Integrin alpha6/genetics,metabolism,physiology Mammary Glands, Human/drug effects,metabolism Mice Mice, Nude Neoplasm Invasiveness Protein Binding Signal Transduction/genetics Tetraspanin 24 Tissue Distribution Transplantation, Heterologous Tumor Cells, Cultured
Chemicals
Antigens, CD CD151 protein, human Cd151 protein, mouse Integrin alpha6 Tetraspanin 24 Epidermal Growth Factor
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Yang Xiuwei H
Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115, USA.
Richardson Andrea L
Torres-Arzayus Maria I
Zhou Pengcheng
Sharma Chandan
Kazarov Alexander R
Andzelm Milena M
Strominger Jack L
Brown Myles
Hemler Martin E
References (50)
50 references, click to expand
  1. Focal adhesion kinase: in command and control of cell motility.
    Nat Rev Mol Cell Biol. 2005 Jan;6(1):56-68 PMID: 15688067
  2. High expression level of alpha 6 integrin in human breast carcinoma is correlated with reduced survival.
    Cancer Res. 1995 Feb 15;55(4):901-6 PMID: 7850807
  3. Autocrine laminin-5 ligates alpha6beta4 integrin and activates RAC and NFkappaB to mediate anchorage-independent survival of mammary tumors.
    J Cell Biol. 2003 Dec 22;163(6):1397-407 PMID: 14691145
  4. Contributions of the alpha6 integrins to breast carcinoma survival and progression.
    Mol Cells. 2004 Apr 30;17(2):203-9 PMID: 15179031
  5. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes.
    Cancer Cell. 2006 Dec;10(6):515-27 PMID: 17157791
  6. CD151, the first member of the tetraspanin (TM4) superfamily detected on erythrocytes, is essential for the correct assembly of human basement membranes in kidney and skin.
    Blood. 2004 Oct 15;104(8):2217-23 PMID: 15265795
  7. Eukaryotic expression cloning with an antimetastatic monoclonal antibody identifies a tetraspanin (PETA-3/CD151) as an effector of human tumor cell migration and metastasis.
    Cancer Res. 1999 Aug 1;59(15):3812-20 PMID: 10447000
  8. Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA-1 and CD151/PETA-3 with alpha3 beta1 integrin localized at endothelial lateral junctions.
    J Cell Biol. 1998 May 4;141(3):791-804 PMID: 9566977
  9. Palmitoylation supports assembly and function of integrin-tetraspanin complexes.
    J Cell Biol. 2004 Dec 20;167(6):1231-40 PMID: 15611341
  10. Alpha 6 beta 4 and alpha 6 beta 1 integrins associate with ErbB-2 in human carcinoma cell lines.
    Exp Cell Res. 1997 Oct 10;236(1):76-85 PMID: 9344587
  11. Akt/PKB signaling in cancer: a function in cell motility and invasion.
    Cell Cycle. 2006 Mar;5(6):603-5 PMID: 16582622
  12. Integrins as receptors for laminins.
    Microsc Res Tech. 2000 Nov 1;51(3):280-301 PMID: 11054877
  13. Deletion of tetraspanin Cd151 results in decreased pathologic angiogenesis in vivo and in vitro.
    Blood. 2007 Feb 15;109(4):1524-32 PMID: 17023588
  14. A novel cysteine cross-linking method reveals a direct association between claudin-1 and tetraspanin CD9.
    Mol Cell Proteomics. 2007 Nov;6(11):1855-67 PMID: 17644758
  15. Rho family proteins and cell migration.
    Biochem Soc Symp. 1999;65:111-23 PMID: 10320936
  16. A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5.
    Mol Biol Cell. 2006 Jun;17(6):2707-21 PMID: 16571677
  17. Kidney failure in mice lacking the tetraspanin CD151.
    J Cell Biol. 2006 Oct 9;175(1):33-9 PMID: 17015618
  18. Tetraspanin CD82 regulates compartmentalisation and ligand-induced dimerization of EGFR.
    J Cell Sci. 2003 Nov 15;116(Pt 22):4557-66 PMID: 14576349
  19. Tetraspanin functions and associated microdomains.
    Nat Rev Mol Cell Biol. 2005 Oct;6(10):801-11 PMID: 16314869
  20. Clinical significance of CD151 gene expression in non-small cell lung cancer.
    Clin Cancer Res. 2001 Dec;7(12):4109-14 PMID: 11751509
  21. CD151 protein expression predicts the clinical outcome of low-grade primary prostate cancer better than histologic grading: a new prognostic indicator?
    Cancer Epidemiol Biomarkers Prev. 2004 Nov;13(11 Pt 1):1717-21 PMID: 15533898
  22. Molecular portraits of human breast tumours.
    Nature. 2000 Aug 17;406(6797):747-52 PMID: 10963602
  23. The tetraspanin superfamily member CD151 regulates outside-in integrin alphaIIbbeta3 signaling and platelet function.
    Blood. 2004 Oct 15;104(8):2368-75 PMID: 15226180
  24. Complexes of tetraspanins with integrins: more than meets the eye.
    J Cell Sci. 2001 Dec;114(Pt 23):4143-51 PMID: 11739647
  25. Protein kinase C-alpha phosphorylation of specific serines in the connecting segment of the beta 4 integrin regulates the dynamics of type II hemidesmosomes.
    Mol Cell Biol. 2004 May;24(10):4351-60 PMID: 15121854
  26. Characterization of mice lacking the tetraspanin superfamily member CD151.
    Mol Cell Biol. 2004 Jul;24(13):5978-88 PMID: 15199151
  27. Tetraspanin microdomains in immune cell signalling and malignant disease.
    Tissue Antigens. 2004 Nov;64(5):533-42 PMID: 15496196
  28. Wound healing is defective in mice lacking tetraspanin CD151.
    J Invest Dermatol. 2006 Mar;126(3):680-9 PMID: 16410781
  29. Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1.
    J Cell Biol. 2006 Jun 5;173(5):795-807 PMID: 16735575
  30. Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology.
    Mol Biol Cell. 2002 Mar;13(3):767-81 PMID: 11907260
  31. EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion.
    J Cell Biol. 2001 Oct 29;155(3):447-58 PMID: 11684709
  32. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis.
    Cell. 2006 Aug 11;126(3):489-502 PMID: 16901783
  33. Human breast cancer MDA-MB-231 cells fail to express the neurofibromin protein, lack its type I mRNA isoform and show accumulation of P-MAPK and activated Ras.
    Cancer Lett. 2001 Oct 30;172(2):159-64 PMID: 11566491
  34. Transmembrane 4 superfamily protein CD151 (PETA-3) associates with beta 1 and alpha IIb beta 3 integrins in haemopoietic cell lines and modulates cell-cell adhesion.
    Biochem J. 1999 Feb 15;338 ( Pt 1):61-70 PMID: 9931299
  35. Targeting the AIB1 oncogene through mammalian target of rapamycin inhibition in the mammary gland.
    Cancer Res. 2006 Dec 1;66(23):11381-8 PMID: 17145884
  36. Deconstructing the molecular portrait of basal-like breast cancer.
    Trends Mol Med. 2006 Nov;12(11):537-44 PMID: 17011236
  37. Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6686-91 PMID: 11390996
  38. Hypoxia regulates cross-talk between Syk and Lck leading to breast cancer progression and angiogenesis.
    J Biol Chem. 2006 Apr 21;281(16):11322-31 PMID: 16474166
  39. Tetraspanin CD151 regulates alpha6beta1 integrin adhesion strengthening.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7616-21 PMID: 12805567
  40. Role of tetraspanins CD9 and CD151 in primary melanocyte motility.
    J Invest Dermatol. 2005 Nov;125(5):1001-9 PMID: 16297202
  41. p56(lck) Controls phosphorylation of filamin (ABP-280) and regulates focal adhesion kinase (pp125(FAK)).
    Cell Biol Int. 2002;26(6):567-71 PMID: 12171035
  42. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates CD151-induced endothelial cell proliferation and cell migration.
    Int J Biochem Cell Biol. 2007;39(2):340-8 PMID: 17045834
  43. PETA-3/CD151, a member of the transmembrane 4 superfamily, is localised to the plasma membrane and endocytic system of endothelial cells, associates with multiple integrins and modulates cell function.
    J Cell Sci. 1999 Mar;112 ( Pt 6):833-44 PMID: 10036233
  44. Control of motile and invasive cell phenotypes by focal adhesion kinase.
    Biochim Biophys Acta. 2004 Jul 5;1692(2-3):77-102 PMID: 15246681
  45. The integrin alpha6beta4 functions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures.
    J Cell Biol. 1997 Dec 29;139(7):1873-84 PMID: 9412479
  46. Hypoxia stimulates carcinoma invasion by stabilizing microtubules and promoting the Rab11 trafficking of the alpha6beta4 integrin.
    Cancer Res. 2005 Apr 1;65(7):2761-9 PMID: 15805276
  47. Beta4 integrin subunit gene expression correlates with tumor size and nuclear grade in early breast cancer.
    Mod Pathol. 2005 Sep;18(9):1165-75 PMID: 15920552
  48. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain.
    Annu Rev Cell Dev Biol. 2003;19:397-422 PMID: 14570575
  49. Potentiation of the ligand-binding activity of integrin alpha3beta1 via association with tetraspanin CD151.
    Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):1939-44 PMID: 15677332
  50. Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion.
    Cell. 1997 Dec 26;91(7):949-60 PMID: 9428518
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2008-05-01
Pages
3204-13
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC4764302
Subset
IM
Grants
NCI NIH HHS · R01 CA042368 · United States
NCI NIH HHS · CA42368 · United States
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