Skip to main content
    • Aa
    • Aa

Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets

  • Christopher S. Stipp (a1)

Within the integrin family of cell adhesion receptors, integrins α3β1, α6β1, α6β4 and α7β1 make up a laminin-binding subfamily. The literature is divided on the role of these laminin-binding integrins in metastasis, with different studies indicating either pro- or antimetastatic functions. The opposing roles of the laminin-binding integrins in different settings might derive in part from their unusually robust associations with tetraspanin proteins. Tetraspanins organise integrins into multiprotein complexes within discrete plasma membrane domains termed tetraspanin-enriched microdomains (TEMs). TEM association is crucial to the strikingly rapid cell migration mediated by some of the laminin-binding integrins. However, emerging data suggest that laminin-binding integrins also promote the stability of E-cadherin-based cell–cell junctions, and that tetraspanins are essential for this function as well. Thus, TEM association endows the laminin-binding integrins with both pro-invasive functions (rapid migration) and anti-invasive functions (stable cell junctions), and the composition of TEMs in different cell types might help determine the balance between these opposing activities. Unravelling the tetraspanin control mechanisms that regulate laminin-binding integrins will help to define the settings where inhibiting the function of these integrins would be helpful rather than harmful, and may create opportunities to modulate integrin activity in more sophisticated ways than simple functional blockade.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets
      Available formats
Re-use permitted under a Creative Commons Licence–by-nc-sa.
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

1 J.D. Humphries , A. Byron and M.J. Humphries (2006) Integrin ligands at a glance. Journal of Cell Science 119, 3901-3903

2 R.O. Hynes (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687

4 C.K. Miranti and J.S. Brugge (2002) Sensing the environment: a historical perspective on integrin signal transduction. Nature Cell Biology 4, E83-90

5 R.W. Gundersen (1987) Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Developmental Biology 121, 423-431

6 A.L. Calof and A.D. Lander (1991) Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti-adhesive. Journal of Cell Biology 115, 779-794

7 R.W. Gundersen (1988) Interference reflection microscopic study of dorsal root growth cones on different substrates: assessment of growth cone-substrate contacts. Journal of Neuroscience Research 21, 298-306

8 T.M. Gomez , F.K. Roche and P.C. Letourneau (1996) Chick sensory neuronal growth cones distinguish fibronectin from laminin by making substratum contacts that resemble focal contacts. Journal of Neurobiology 29, 18-34

9 J. Gu (2001) Laminin-10/11 and fibronectin differentially regulate integrin-dependent Rho and Rac activation via p130(Cas)-CrkII-DOCK180 pathway. Journal of Biological Chemistry 276, 27090-27097

10 D.E. Frank and W.G. Carter (2004) Laminin 5 deposition regulates keratinocyte polarization and persistent migration. Journal of Cell Science 117, 1351-1363

11 H. Zhou and R.H. Kramer (2005) Integrin engagement differentially modulates epithelial cell motility by RhoA/ROCK and PAK1. Journal of Biological Chemistry 280, 10624-10635

12 N.E. Winterwood (2006) A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5. Molecular Biology of the Cell 17, 2707-2721

13 R. Nishiuchi (2006) Ligand-binding specificities of laminin-binding integrins: a comprehensive survey of laminin-integrin interactions using recombinant alpha3beta1, alpha6beta1, alpha7beta1 and alpha6beta4 integrins. Matrix Biology 25, 189-197

14 R.J. Faull (1994) Stimulation of integrin-mediated adhesion of T lymphocytes and monocytes: two mechanisms with divergent biological consequences. Journal of Experimental Medicine 179, 1307-1316

15 A. Kern (1993) Interaction of type IV collagen with the isolated integrins alpha 1 beta 1 and alpha 2 beta 1. European Journal of Biochemistry 215, 151-159

16 T. Yoshimasu (2004) Increased expression of integrin alpha3beta1 in highly brain metastatic subclone of a human non-small cell lung cancer cell line. Cancer Science 95, 142-148

17 H. Takatsuki (2004) Adhesion of gastric carcinoma cells to peritoneum mediated by alpha3beta1 integrin (VLA-3). Cancer Research 64, 6065-6070

18 H. Wang (2004) Tumor cell alpha3beta1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. Journal of Cell Biology 164, 935-941

19 T. Kawataki (2007) Laminin isoforms and their integrin receptors in glioma cell migration and invasiveness: Evidence for a role of alpha5-laminin(s) and alpha3beta1 integrin. Experimental Cell Research 313, 3819-3831

20 S. Dedhar (1993) Specific alterations in the expression of alpha 3 beta 1 and alpha 6 beta 4 integrins in highly invasive and metastatic variants of human prostate carcinoma cells selected by in vitro invasion through reconstituted basement membrane. Clinical and Experimental Metastasis 11, 391-400

21 M. Bockhorn (2004) Differential gene expression in metastasizing cells shed from kidney tumors. Cancer Research 64, 2469-2473

22 C. Margadant (2009) Integrin {alpha}3{beta}1 inhibits directional migration and wound re-epithelialization in the skin. Journal of Cell Science 122, 278-288

23 W.G. Carter (1990) The role of integrins alpha 2 beta 1 and alpha 3 beta 1 in cell-cell and cell-substrate adhesion of human epidermal cells. Journal of Cell Biology 110, 1387-1404

24 P.D. Lampe (1998) Cellular interaction of integrin alpha3beta1 with laminin 5 promotes gap junctional communication. Journal of Cell Biology 143, 1735-1747

26 K.M. Hodivala-Dilke (1998) Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. Journal of Cell Biology 142, 1357-1369

27 N.T. Chartier (2006) Laminin-5-integrin interaction signals through PI 3-kinase and Rac1b to promote assembly of adherens junctions in HT-29 cells. Journal of Cell Science 119, 31-46

29 M. Shigeta (2003) CD151 regulates epithelial cell-cell adhesion through PKC- and Cdc42-dependent actin cytoskeletal reorganization. Journal of Cell Biology 163, 165-176

30 A. Koenig (2006) Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells. Cancer Research 66, 4662-4671

31 Y. Wang (2006) Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras. Proceedings of the National Academy of Sciences of the United States of America 103, 1774-1779

32 J. de Rooij (2005) Integrin-dependent actomyosin contraction regulates epithelial cell scattering. Journal of Cell Biology 171, 153-164

34 J.B. Weitzman , M.E. Hemler and P. Brodt (1996) Reduction of tumorigenicity by alpha 3 integrin in a rhabdomyosarcoma cell line. Cell Adhesion and Communication 4, 41-52

35 Y. Kim (2009) Integrin alpha3beta1-dependent beta-catenin phosphorylation links epithelial Smad signaling to cell contacts. Journal of Cell Biology 184, 309-322

37 D. Padua and J. Massagué (2009) Roles of TGFbeta in metastasis. Cell Research 19, 89-102

38 E.A. Lipscomb and A.M. Mercurio (2005) Mobilization and activation of a signaling competent alpha6beta4integrin underlies its contribution to carcinoma progression. Cancer and Metastasis Reviews 24, 413-423

39 F.G. Giancotti (2007) Targeting integrin beta4 for cancer and anti-angiogenic therapy. Trends in Pharmacological Sciences 28, 506-511

40 K. Wilhelmsen , S.H. Litjens and A. Sonnenberg (2006) Multiple functions of the integrin alpha6beta4 in epidermal homeostasis and tumorigenesis. Molecular and Cellular Biology 26, 2877-2886

41 D.M. Owens (2003) Suprabasal alpha6beta4 integrin expression in epidermis results in enhanced tumourigenesis and disruption of TGFbeta signalling. Journal of Cell Science 116, 3783-3791

42 M. Dajee (2003) NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 421, 639-643

43 A.E. Cress (1995) The alpha 6 beta 1 and alpha 6 beta 4 integrins in human prostate cancer progression. Cancer and Metastasis Reviews 14, 219-228

44 M.O. Ports (2009) Extracellular engagement of alpha6 integrin inhibited urokinase-type plasminogen activator-mediated cleavage and delayed human prostate bone metastasis. Cancer Research 69, 5007-5014

45 T.E. King (2008) The role of alpha 6 integrin in prostate cancer migration and bone pain in a novel xenograft model. PLoS One 3, e3535

46 K. Raymond (2007) Dual Role of alpha6beta4 integrin in epidermal tumor growth: tumor-suppressive versus tumor-promoting function. Molecular Biology of the Cell 18, 4210-4221

47 E. Hintermann (2005) Integrin alpha6beta4-erbB2 complex inhibits haptotaxis by up-regulating E-cadherin cell-cell junctions in keratinocytes. Journal of Biological Chemistry 280, 8004-8015

50 T. Velling (1996) Distinct alpha 7A beta 1 and alpha 7B beta 1 integrin expression patterns during mouse development: alpha 7A is restricted to skeletal muscle but alpha 7B is expressed in striated muscle, vasculature, and nervous system. Developmental Dynamics 207, 355-371

52 B. Ren (2007) Analysis of integrin alpha7 mutations in prostate cancer, liver cancer, glioblastoma multiforme, and leiomyosarcoma. Journal of the National Cancer Institute 99, 868-880

53 G. Min (2006) Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. Journal of Cell Biology 173, 975-983

54 M. Seigneuret (2006) Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophysical Journal 90, 212-227

55 M. Seigneuret (2001) Structure of the tetraspanin main extracellular domain. A partially conserved fold with a structurally variable domain insertion. Journal of Biological Chemistry 276, 40055-40064

56 K. Kitadokoro (2001) CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO Journal 20, 12-18

57 O.V. Kovalenko (2004) Evidence for specific tetraspanin homodimers: inhibition of palmitoylation makes cysteine residues available for cross-linking. Biochemical Journal 377, 407-417

58 O.V. Kovalenko (2005) Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Structural Biology 5, 11

59 R. Bari (2009) Transmembrane interactions are needed for KAI1/CD82-mediated suppression of cancer invasion and metastasis. American Journal of Pathology 174, 647-660

60 S. Nydegger (2006) Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1. Journal of Cell Biology 173, 795-807

61 O. Barreiro (2008) Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. Journal of Cell Biology 183, 527-542

62 C. Espenel (2008) Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. Journal of Cell Biology 182, 765-776

63 M. Yanez-Mo (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends in Cell Biology 19, 434-446

64 F. Berditchevski (2002) Expression of the palmitoylation-deficient CD151 weakens the association of alpha 3 beta 1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling. Journal of Biological Chemistry 277, 36991-37000

65 S. Charrin (2002) Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Letters 516, 139-144

66 X. Yang (2002) Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Molecular Biology of the Cell 13, 767-781

67 X. Yang (2004) Palmitoylation supports assembly and function of integrin-tetraspanin complexes. Journal of Cell Biology 167, 1231-1240

68 R.L. Yauch (1998) Highly stoichiometric, stable, and specific association of integrin alpha3beta1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Molecular Biology of the Cell 9, 2751-2765

69 R.L. Yauch (2000) Direct extracellular contact between integrin alpha(3)beta(1) and TM4SF protein CD151. Journal of Biological Chemistry 275, 9230-9238

70 V. Serru (1999) Selective tetraspan-integrin complexes (CD81/alpha4beta1, CD151/alpha3beta1, CD151/alpha6beta1) under conditions disrupting tetraspan interactions. Biochemical Journal 340, 103-111

71 A.R. Kazarov (2002) An extracellular site on tetraspanin CD151 determines alpha 3 and alpha 6 integrin-dependent cellular morphology. Journal of Cell Biology 158, 1299-1309

73 F. Berditchevski (2001) Analysis of the CD151-alpha3beta1 integrin and CD151-tetraspanin interactions by mutagenesis. Journal of Biological Chemistry 276, 41165-41174

74 C.S. Stipp , T.V. Kolesnikova and M.E. Hemler (2003) EWI-2 regulates alpha3beta1 integrin-dependent cell functions on laminin-5. Journal of Cell Biology 163, 1167-1177

75 S. Charrin (2003) Multiple levels of interactions within the tetraspanin web. Biochemical and Biophysical Research Communications 304, 107-112

76 X.H. Yang (2008) CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Research 68, 3204-3213

77 Y. Takeda (2007) Deletion of tetraspanin Cd151 results in decreased pathologic angiogenesis in vivo and in vitro. Blood 109, 1524-1532

78 M. Yamada (2008) The tetraspanin CD151 regulates cell morphology and intracellular signaling on laminin-511. FEBS Journal 275, 3335-3351

79 M. André (2006) Proteomic analysis of the tetraspanin web using LC-ESI-MS/MS and MALDI-FTICR-MS. Proteomics 6, 1437-1449

80 F. Le Naour (2006) Profiling of the tetraspanin web of human colon cancer cells. Molecular and Cellular Proteomics 5, 845-857

81 O.V. Kovalenko , X.H. Yang and M.E. Hemler (2007) A novel cysteine cross-linking method reveals a direct association between claudin-1 and tetraspanin CD9. Molecular and Cellular Proteomics 6, 1855-1867

82 M.E. Hemler (2005) Tetraspanin functions and associated microdomains. Nature Reviews Molecular Cell Biology 6, 801-811

83 S. Levy and T. Shoham (2005) The tetraspanin web modulates immune-signalling complexes. Nature Reviews Immunology 5, 136-148

84 X.A. Zhang , A.L. Bontrager and M.E. Hemler (2001) Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific beta(1) integrins. Journal of Biological Chemistry 276, 25005-25013

85 F. Berditchevski (1997) A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. Journal of Biological Chemistry 272, 2595-2598

86 R.L. Yauch and M.E. Hemler (2000) Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphoinositide 4-kinase. Biochemical Journal 351, 629-637

87 Y. Chang and S.C. Finnemann (2007) Tetraspanin CD81 is required for the alpha v beta5-integrin-dependent particle-binding step of RPE phagocytosis. Journal of Cell Science 120, 3053-3063

88 M. Sala-Valdes (2006) EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins. Journal of Biological Chemistry 281, 19665-19675

89 C.S. Stipp , T.V. Kolesnikova and M.E. Hemler (2003) Functional domains in tetraspanin proteins. Trends in Biochemical Sciences 28, 106-112

91 B.A. Rous (2002) Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Molecular Biology of the Cell 13, 1071-1082

92 N. Latysheva (2006) Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63. Molecular and Cellular Biology 26, 7707-7718

94 K.D. Little , M.E. Hemler and C.S. Stipp (2004) Dynamic regulation of a GPCR-tetraspanin-G protein complex on intact cells: central role of CD81 in facilitating GPR56-Galpha q/11 association. Molecular Biology of the Cell 15, 2375-2387

95 S. Charrin (2009) Lateral organization of membrane proteins: tetraspanins spin their web. Biochemical Journal 420, 133-154

97 J. Kotha (2008) Tetraspanin CD9 regulates beta 1 integrin activation and enhances cell motility to fibronectin via a PI-3 kinase-dependent pathway. Experimental Cell Research 314, 1811-1822

98 S. Fitter (1999) 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. Biochemical Journal 338, 61-70

99 R. Nishiuchi (2005) Potentiation of the ligand-binding activity of integrin alpha3beta1 via association with tetraspanin CD151. Proceedings of the National Academy of Sciences of the United States of America 102, 1939-1944

100 N. Pampori (1999) Mechanisms and consequences of affinity modulation of integrin alpha(V)beta(3) detected with a novel patch-engineered monovalent ligand. Journal of Biological Chemistry 274, 21609-21616

101 L.M. Lau (2004) The tetraspanin superfamily member CD151 regulates outside-in integrin alphaIIbbeta3 signaling and platelet function. Blood 104, 2368-2375

102 S.M. Geary (2008) The role of the tetraspanin CD151 in primary keratinocyte and fibroblast functions: implications for wound healing. Experimental Cell Research 314, 2165-2175

103 M. Hasegawa (2007) CD151 dynamics in carcinoma-stroma interaction: integrin expression, adhesion strength and proteolytic activity. Laboratory Investigation 87, 882-892

104 J. Lammerding (2003) Tetraspanin CD151 regulates alpha6beta1 integrin adhesion strengthening. Proceedings of the National Academy of Sciences of the United States of America 100, 7616-7621

105 N.D. Gallant , K.E. Michael and A.J. Garcia (2005) Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Molecular Biology of the Cell 16, 4329-4340

106 E. Puklin-Faucher and M.P. Sheetz (2009) The mechanical integrin cycle. Journal of Cell Science 122, 179-186

107 S.W. Feigelson (2003) The CD81 tetraspanin facilitates instantaneous leukocyte VLA-4 adhesion strengthening to vascular cell adhesion molecule 1 (VCAM-1) under shear flow. Journal of Biological Chemistry 278, 51203-51212

108 B. He (2005) Tetraspanin CD82 attenuates cellular morphogenesis through down-regulating integrin alpha6-mediated cell adhesion. Journal of Biological Chemistry 280, 3346-3354

109 S.C. Sridhar and C.K. Miranti (2006) Tetraspanin KAI1/CD82 suppresses invasion by inhibiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene 25, 2367-2378

110 L. Liu (2007) Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. Journal of Biological Chemistry 282, 31631-31642

111 C. Xu (2009) CD82 endocytosis and cholesterol-dependent reorganization of tetraspanin webs and lipid rafts. FASEB Journal 10.1096/fj.1008-123414

112 R. Sadej (2009) CD151 regulates tumorigenesis by modulating the communication between tumor cells and endothelium. Molecular Cancer Research 7, 787-798

113 X.A. Zhang (2003) Requirement of the p130CAS-Crk coupling for metastasis suppressor KAI1/CD82-mediated inhibition of cell migration. Journal of Biological Chemistry 278, 27319-27328

114 J.L. Johnson (2009) Tetraspanin CD151 regulates RhoA activation and the dynamic stability of carcinoma cell-cell contacts. Journal of Cell Science 122, 2263-2273

115 N. Chattopadhyay (2003) alpha3beta1 integrin-CD151, a component of the cadherin-catenin complex, regulates PTPmu expression and cell-cell adhesion. Journal of Cell Biology 163, 1351-1362

116 S. Sawada (2003) The tetraspanin CD151 functions as a negative regulator in the adhesion-dependent activation of Ras. Journal of Biological Chemistry 278, 26323-26326

117 N.K. Noren (2001) Cadherin engagement regulates Rho family GTPases. Journal of Biological Chemistry 276, 33305-33308

118 M. Furuya (2005) Down-regulation of CD9 in human ovarian carcinoma cell might contribute to peritoneal dissemination: morphologic alteration and reduced expression of beta1 integrin subsets. Cancer Research 65, 2617-2625

119 M. Abe (2008) A novel function of CD82/KAI-1 on E-cadherin-mediated homophilic cellular adhesion of cancer cells. Cancer Letters 266, 163-170

121 C.K. Miranti (2009) Controlling cell surface dynamics and signaling: how CD82/KAI1 suppresses metastasis. Cellular Signalling 21, 196-211

122 L.M. Sterk (2000) The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin alpha6beta4 and may regulate the spatial organization of hemidesmosomes. Journal of Cell Biology 149, 969-982

123 M.E. Hemler (2008) Targeting of tetraspanin proteins–potential benefits and strategies. Nature Reviews Drug Discovery 7, 747-758

124 E. Hintermann (2001) Inhibitory role of alpha 6 beta 4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on alpha 3 beta 1 integrin. Journal of Cell Biology 153, 465-478

125 S.N. Nikolopoulos (2004) Integrin beta4 signaling promotes tumor angiogenesis. Cancer Cell 6, 471-483

127 H. Hashida (2003) Clinical significance of transmembrane 4 superfamily in colon cancer. British Journal of Cancer 89, 158-167

129 A. Zijlstra (2008) The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 13, 221-234

130 N. Sachs (2006) Kidney failure in mice lacking the tetraspanin CD151. Journal of Cell Biology 175, 33-39

131 V. Karamatic Crew (2004) 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 104, 2217-2223

132 R.M. Baleato (2008) Deletion of CD151 results in a strain-dependent glomerular disease due to severe alterations of the glomerular basement membrane. American Journal of Pathology 173, 927-937

133 C. Sharma , X.H. Yang and M.E. Hemler (2008) DHHC2 affects palmitoylation, stability, and functions of tetraspanins CD9 and CD151. Molecular Biology of the Cell 19, 3415-3425

134 Z. Jarikji (2009) The tetraspanin Tm4sf3 is localized to the ventral pancreas and regulates fusion of the dorsal and ventral pancreatic buds. Development 136, 1791-1800

135 T. Takeda (2007) Adenoviral transduction of MRP-1/CD9 and KAI1/CD82 inhibits lymph node metastasis in orthotopic lung cancer model. Cancer Research 67, 1744-1749

136 Y.C. Tsai (2007) The ubiquitin ligase gp78 promotes sarcoma metastasis by targeting KAI1 for degradation. Nature Medicine 13, 1504-1509

137 P. Guédat and F. Colland (2007) Patented small molecule inhibitors in the ubiquitin proteasome system. BMC Biochemistry 8 (Suppl 1), S14

138 M. Morini (2000) The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. International Journal of Cancer 87, 336-342

139 C. Sakakura (2002) Differential gene expression profiles of gastric cancer cells established from primary tumour and malignant ascites. British Journal of Cancer 87, 1153-1161

140 H. Ura (1998) Separate functions of alpha2beta1 and alpha3beta1 integrins in the metastatic process of human gastric carcinoma. Surgery Today 28, 1001-1006

141 A. Kurokawa (2008) Diagnostic value of integrin alpha3, beta4, and beta5 gene expression levels for the clinical outcome of tongue squamous cell carcinoma. Cancer 112, 1272-1281

142 M. Nagata (2003) Identification of potential biomarkers of lymph node metastasis in oral squamous cell carcinoma by cDNA microarray analysis. International Journal of Cancer 106, 683-689

143 O.H. Dyce (2002) Integrins in head and neck squamous cell carcinoma invasion. Laryngoscope 112, 2025-2032

144 M. Shinohara (1999) Expression of integrins in squamous cell carcinoma of the oral cavity. Correlations with tumor invasion and metastasis. American Journal of Clinical Pathology 111, 75-88

145 G. Giannelli (2002) Transforming growth factor-beta1 triggers hepatocellular carcinoma invasiveness via alpha3beta1 integrin. American Journal of Pathology 161, 183-193

146 P.G. Natali (1993) Integrin expression in cutaneous malignant melanoma: association of the alpha 3/beta 1 heterodimer with tumor progression. International Journal of Cancer 54, 68-72

147 I.G. Yoshinaga (1993) Role of alpha 3 beta 1 and alpha 2 beta 1 integrins in melanoma cell migration. Melanoma Research 3, 435-441

148 H. Nishimori (2002) A novel nude mouse model of liver metastasis and peritoneal dissemination from the same human pancreatic cancer line. Pancreas 24, 242-250

149 G.P. Gui (1995) Integrin expression in primary breast cancer and its relation to axillary nodal status. Surgery 117, 102-108

150 G.P. Gui (1996) Integrin expression in breast cancer cytology: a novel predictor of axillary metastasis. European Journal of Surgical Oncology 22, 254-258

152 H. Hashida (2002) Integrin alpha3 expression as a prognostic factor in colon cancer: association with MRP-1/CD9 and KAI1/CD82. International Journal of Cancer 97, 518-525

153 I. Sordat (2002) Complementary DNA arrays identify CD63 tetraspanin and alpha3 integrin chain as differentially expressed in low and high metastatic human colon carcinoma cells. Laboratory Investigation 82, 1715-1724

154 S. Miyamoto (2001) Loss of motility-related protein 1 (MRP1/CD9) and integrin alpha3 expression in endometrial cancers. Cancer 92, 542-548

156 T. Ohara (2009) Integrin expression levels correlate with invasion, metastasis and prognosis of oral squamous cell carcinoma. Pathology Oncology Research 15, 429-436

158 M.Z. Gilcrease (2009) Coexpression of alpha6beta4 integrin and guanine nucleotide exchange factor Net1 identifies node-positive breast cancer patients at high risk for distant metastasis. Cancer Epidemiology Biomarkers and Prevention 18, 80-86

159 S. Lu (2008) Analysis of integrin beta4 expression in human breast cancer: association with basal-like tumors and prognostic significance. Clinical Cancer Research 14, 1050-1058

162 C. Herold-Mende (2001) Metastatic growth of squamous cell carcinomas is correlated with upregulation and redistribution of hemidesmosomal components. Cell and Tissue Research 306, 399-408

165 X. Wan (2009) Beta4 integrin promotes osteosarcoma metastasis and interacts with ezrin. Oncogene 28, 3401-3411

167 H. Sawai (2006) Interleukin-1alpha enhances the aggressive behavior of pancreatic cancer cells by regulating the alpha6beta1-integrin and urokinase plasminogen activator receptor expression. BMC Cell Biology 7, 8

168 S. Kitajiri (2002) Increased expression of integrin beta-4 in papillary thyroid carcinoma with gross lymph node metastasis. Pathology International 52, 438-441

169 S.R. Elshaw (2001) A comparison of ocular melanocyte and uveal melanoma cell invasion and the implication of alpha1beta1, alpha4beta1 and alpha6beta1 integrins. British Journal of Ophthalmology 85, 732-738

170 D. Schadendorf (1993) Tumour progression and metastatic behaviour in vivo correlates with integrin expression on melanocytic tumours. Journal of Pathology 170, 429-434

172 V. Givant-Horwitz (2003) Expression of the 67 kDa laminin receptor and the alpha6 integrin subunit in serous ovarian carcinoma. Clinical and Experimental Metastasis 20, 599-609

173 J.E. Bridges (1995) Expression of integrin adhesion molecules in normal ovary and epithelial ovarian tumors. International Journal of Gynecological Cancer 5, 187-192

174 W. Guo (2006) Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 126, 489-502

175 P. Gassmann (2009) Metastatic tumor cell arrest in the liver-lumen occlusion and specific adhesion are not exclusive. International Journal of Colorectal Disease 24, 851-858

176 A. Enns (2004) Integrins can directly mediate metastatic tumor cell adhesion within the liver sinusoids. Journal of Gastrointestinal Surgery 8, 1049-1059; discussion 1060

177 J.H. Robertson (2009) Functional blocking of specific integrins inhibit colonic cancer migration. Clinical and Experimental Metastasis 26, 769-780

178 H. Yamamoto (1996) Abrogation of lung metastasis of human fibrosarcoma cells by ribozyme-mediated suppression of integrin alpha6 subunit expression. International Journal of Cancer 65, 519-524

180 P. Ruiz (1993) Suppression of mouse melanoma metastasis by EA-1, a monoclonal antibody specific for alpha 6 integrins. Cell Adhesion and Communication 1, 67-81

181 L. Trusolino , A. Bertotti and P.M. Comoglio (2001) A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell 107, 643-654

182 R. Vogelmann (1999) Integrin alpha6beta1 role in metastatic behavior of human pancreatic carcinoma cells. International Journal of Cancer 80, 791-795

M. Zöller (2009) Tetraspanins: push and pull in suppressing and promoting metastasis. Nature Reviews Cancer 9, 40-55

F. Berditchevski and E. Odintsova (2007) Tetraspanins as regulators of protein trafficking. Traffic 8, 89-96

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Expert Reviews in Molecular Medicine
  • ISSN: -
  • EISSN: 1462-3994
  • URL: /core/journals/expert-reviews-in-molecular-medicine
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Full text views

Total number of HTML views: 10
Total number of PDF views: 145 *
Loading metrics...

Abstract views

Total abstract views: 170 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 26th May 2017. This data will be updated every 24 hours.