Tetraspanin-enriched microdomains and hepatocellular carcinoma progression

Cancer Letters

Volumn 351, Issue 1, 2014, Pages 23-29

  Mazzocca, Antonio ^a,b   Tahmasebi Birgani, Maryam ^c   Sabbà, Carlo ^a   Carloni, Vinicio ^d  

^a UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^b NATIONAL INSTITUTE FOR DIGESTIVE DISEASES   (Italy)

^c AHVAZ JUNDISHAPUR UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Cancer heterogeneity; Cancer progression; Hepatocellular carcinoma; Metastasis; Tetraspanins

Indexed keywords

CD151 ANTIGEN; CD81 ANTIGEN; INTEGRIN; PHOSPHOINOSITIDE 4 KINASE; PHOSPHOTRANSFERASE; TETRASPANIN; UNCLASSIFIED DRUG;

ANTIGEN DETECTION; ANTIGEN FUNCTION; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; CELL VIABILITY; DISEASE ACTIVITY; DISEASE ASSOCIATION; HUMAN; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SHORT SURVEY;

CANCER HETEROGENEITY; CANCER PROGRESSION; HEPATOCELLULAR CARCINOMA; METASTASIS; TETRASPANINS;

CARCINOGENESIS; CARCINOMA, HEPATOCELLULAR; HUMANS; LIVER NEOPLASMS; MEMBRANE MICRODOMAINS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); TETRASPANINS;

EID: 84903714008     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.05.016     Document Type: Review

References (85)

1. Deuffic S., Poynard T., Buffat L., Valleron A.J. Trends in primary liver cancer. Lancet 1998, 351:214-215.
2. La Vecchia C., Lucchini F., Franceschi S., Negri E., Levi F. Trends in mortality from primary liver cancer in Europe. Eur. J. Cancer 2000, 36:909-915.
3. Schutte K., Bornschein J., Malfertheiner P. Hepatocellular carcinoma epidemiological trends and risk factors. Dig. Dis. 2009, 27:80-92.
4. Lok A.S., Seeff L.B., Morgan T.R., Di Bisceglie A.M., Sterling R.K., Curto T.M., et al. Incidence of hepatocellular carcinoma and associated risk factors in hepatitis C related advanced liver disease. Gastroenterology 2009, 136:138-148.
5. Fattovich G., Stroffolini T., Zagni I., Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004, 127(Suppl. 1):S35-S50.
6. Carloni V., Luong T.V., Rombouts K. Hepatic stellate cells and ECM in HCC: more complicated than ever. Liver Int. 2014, 10.1111/liv.12465.
7. Kanwal F., Hoang T., Kramer J.R., Asch S.M., Goetz M.B., Zeringue A., et al. Increasing prevalence of HCC and cirrhosis in patients with chronic hepatitis C virus infection. Gastroenterology 2011, 140:1182-1188. e1.
8. El-Serag H.B., Marrero J.A., Rudolph K.L., Reddy K.R. Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology 2008, 134:1752-1763.
9. El-Serag H.-B., Rudolph K.L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007, 132:2557-2576.
10. Yuen M.F., Tanaka Y., Fong D.Y., Fung J., Wong D.K., Yuen J.C., et al. Independent risk factors and predictive score for the development of hepatocellular carcinoma in chronic hepatitis B. J. Hepatol. 2009, 50:80-88.
11. Rombouts K., Carloni V. The fibrotic microenvironment as a heterogeneity facet of hepatocellular carcinoma. Fibrogenesis. Tissue Repair 2013, 6:17-22.
12. Wilkens L., Flemming P., Gebel M., Bleck J., Terkamp C., Wingen L., et al. Induction of aneuploidy by increasing chromosomal instability during dedifferentiation of hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 2004, 101:1309-1314.
13. Woo H.G., Park E.S., Thorgeirsson S.S., Kim Y.J. Exploring genomic profiles of hepatocellular carcinoma. Mol. Carcinog 2011, 50:235-243.
14. Wurmbach E., Chen Y.E., Khitrov G., Zhang W., Roayaie S., Schwartz M., et al. Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular Carcinoma. Hepatology 2007, 45:938-947.
15. Hoshida Y., Villanueva A., Kobayashi M., Peix J., Chiang D.Y., Camargo A., et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N. Engl. J. Med. 2008, 359:1995-2004.
16. Hoshida Y., Villanueva A., Sangiovanni A., Sole M., Hur C., Andersson K.L., et al. Prognostic gene expression signature for patients with hepatitis C-related early stage cirrhosis. Gastroenterology 2013, 144:1024-1030.
17. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., et al. Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
18. Marusyk A., Almendro V., Polyak K. Intra-tumour heterogeneity: a looking glass for cancer?. Nat. Rev. Cancer 2012, 12:323-334.
19. Li Y., Tang Z.Y., Hou J.X. Hepatocellular carcinoma: insight from animal models. Nat. Rev. Gastroenterol. Hepatol. 2011, 9:32-43.
20. Farazi P.A., DePinho R.A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat. Rev. Cancer 2006, 6:674-687.
21. Tao Y., Ruan J., Yeh S.H., Lu X., Wang Y., Zhai W., et al. Rapid growth of a hepatocellular carcinoma and the driving mutations revealed by cell-population genetic analysis of whole-genome data. Proc. Natl. Acad. Sci. USA 2011, 108:12042-12047.
22. Gerlinger M., Swanton C. How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. Br. J. Cancer 2010, 103:1139-1143.
23. Tarin D. Cell and tissue interactions in carcinogenesis and metastasis and their clinical significance. Semin. Cancer Biol. 2011, 21:72-82.
24. Sieber J.J., Willig K.I., Kutzner C., Gerding-Reimers C., Harke B., Donnert G., et al. Anatomy and dynamics of a supramolecular membrane protein cluster. Science 2007, 317:1072-1076.
25. Brock A., Chang H., Huang S. Non-genetic heterogeneity a mutation-independent driving force for the somatic evolution of tumours. Nature Rev. Genetics 2009, 10:336-342.
26. Lee A.J., Endesfelder D., Rowan A.J., Walther A., Birkbak N.J., Futreal P.A., et al. Chromosomal instability confers intrinsic multidrug resistance. Cancer Res. 2011, 71:1858-1870.
27. Yáñez-Mó M., Barreiro O., Gordon-Alonso M., Sala-Valdés M., Sánchez-Madrid F. Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol. 2009, 19:434-446.
28. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1:31-39.
29. Zheng Y.Z., Foster L.J. Biochemical and proteomic approaches for the study of membrane microdomains. J. Proteomics 2009, 72:12-22.
30. Carloni V., Mazzocca A., Mello T., Galli A., Capaccioli S. Cell fusion promotes chemoresistance in metastatic colon carcinoma. Oncogene 2013, 32:2649-2660.
31. Hemler M.E. Targeting of tetraspanin proteins, potential benefits and strategies. Nat. Drug Discov. 2008, 7:747-758.
32. Claas C., Stipp C.S., Hemler M.E. Evaluation of prototype TM4SF protein complexes and their relation to lipid rafts. J. Biol. Chem. 2001, 276:7974-7984.
33. Yauch R.L., Berditchevski F., Harler M.B., Reichner J., Hemler M.E. Highly stoichiometric, stable and specific association of integrin α3β1 with CD151 provides a major link to phosphatidylinositol 4-kinase and may regulate cell migration. Mol. Biol. Cell 1998, 9:2751-2765.
34. Kovalenko O.V., Metcalf D.G., DeGrado W.F., Hemler M.E. Structural organization and interactions of transmembrane domains in tetraspanin proteins. BMC Struct. Biol. 2005, 5:11.
35. Yunta M., Lazo P.A. Tetraspanin proteins as organisers of membrane microdomains and signaling complexes. Cell. Signal. 2003, 15:559-564.
36. Zoller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nat. Rev. Cancer 2009, 9:40-55.
37. Oren R., Takahashi S., Doss C., Levy R., Levy S. TAPA-1, the target of an antiproliferative antibody, defines a new family of transmembrane proteins. Mol. Cell. Biol. 1990, 10:4007-4015.
38. Mazzocca A., Carloni V., Sciammetta S., Cordella C., Pantaleo P., Caldini A., et al. Expression of transmembrane 4 superfamily (TM4SF) proteins and their role in hepatic stellate cell motility and wound healing migration. J. Hepatol. 2002, 37:322-330.
39. Mazzocca A., Carloni V., Sciammetta S.C., Cosmi L., Annunziato F., Harada T., et al. Binding of hepatitis C virus envelope protein E2 to CD81 up-regulates matrix metalloproteinase - 2 in human hepatic stellate cells. J. Biol. Chem. 2005, 280:11329-11339.
40. Carloni V., Mazzocca A., Ravichandran K.S. Tetraspanin CD81 is linked to ERK/MAPKinase signaling by Shc in liver tumor cells. Oncogene 2004, 23:1566-1574.
41. Hancock J.F. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 2006, 7:456-462.
42. Inoue G., Horiike N., Onji M. The CD81 expression in liver in hepatocellular carcinoma. Int. J. Mol. Med. 2001, 27:67-71.
43. Schöniger-Hekele M., Hänel S., Wrba F., Müller C. Hepatocellular carcinoma survival and clinical characteristics in relation to various histologic molecular markers in Western patients. Liver Int. 2005, 25:62-69.
44. Mazzocca A., Liotta F., Carloni V. Tetraspanin CD81-regulated cell motility plays a critical role in intrahepatic metastasis of hepatocellular carcinoma. Gastroenterology 2008, 135:244-256.
45. Mazzocca A., Carloni V. The metastatic process: methodological advances and pharmacological challenges. Curr. Med. Chem. 2009, 16:1704-1717.
46. Hemler M.E. Tetraspanin proteins promote multiple cancer stages. Nat. Rev. Cancer 2014, 14:49-60.
47. Testa J.E., Brooks P.C., Lin J.M., Quigley J.P. 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, 59:3812-3820.
48. Zijlstra A., Lewis J., Degryse B., Stuhlmann H., Quigley J.P. The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 2008, 13:221-234.
49. Shi G.M., KE A.W., Zhou J., Wang X.Y., Xu Y., Ding Z.B., et al. CD151 modulates expression of matrix metalloproteinase 9 and promotes neoangiogenesis and progression of hepatocellular carcinoma. Hepatology 2010, 52:183-196.
50. Ke A.W., Shi G.M., Zhou J., Wu F.Z., Ding Z.B., Hu M.Y., et al. Role of overexpression of CD151 and/or c-Met in predicting prognosis of hepatocellular carcinoma. Hepatology 2009, 49:491-503.
51. Ke A.W., Shi G.M., Zhou J., Huang X.Y., Shi Y.H., Ding Z.B., et al. CD151 amplifies signaling by integrin α6β1 to PI3K and induces the epithelial-mesenchymal transition in HCC cells. Gastroenterology 2011, 140:1629-1641.
52. Gesierich S., Berezovskiy I., Ryschich E., Zoller M. Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res. 2006, 66:7083-7094.
53. Kanetaka K., Sakamoto M., Yamamoto Y., Takamura M., Kanematsu T., Hirohashi S. Possible involvement of tetraspanin CO-029 in hematogenous intrahepatic metastasis of liver cancer cells. J. Gastroenterol. Hepatol. 2003, 18:1309-1314.
54. Guo X.Z., Friess H., Di Mola F.F., Heinicke J.M., Abou-Shady M., Graber H.U., et al. KAI1, a new metastasis suppressor gene, is reduced in metastatic hepatocellular carcinoma. Hepatology 1998, 28:1481-1488.
55. Abe M., Sugiura T., Takahashi M., Ishii K., Shimoda M., Shirasuna K. A novel function of CD82/KAI-1 on E-cadherin-mediated homophilic cellular adhesion of cancer cells. Cancer Lett. 2008, 266:163-170.
56. Bandyopadhyay S., Zhan R., Chaudhuri A., Watabe M., Pai S.K., Hirota S., et al. Interaction of KAI1 on tumor cells with DARC on vascular endothelium leads to metastasis suppression. Nat. Med. 2006, 12:933-938.
57. Yanez-Mo M., Gutierrez-Lopez M.D., Cabanas C. Functional interplay between tetraspanins and proteases. Cell. Mol. Life Sci. 2011, 68:3323-3335.
58. Waugh M.G. Phosphatidylinositol 4-kinases, phosphatidylinositol 4-phosphate and cancer. Cancer Lett. 2012, 325:125-131.
59. Clayton E.L., Minogue S., Waugh M.G. Mammalian phosphatidylinositol 4-kinases as modulators of membrane trafficking and lipid signaling networks. Prog. Lipid. Res. 2013, 52:294-304.
60. Balla A., Balla T. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 2006, 16:351-361.
61. Minogue S., Waugh M.G. The phosphatidylinositol 4-kinases: do not call it a comeback. Subcell. Biochem. 2012, 58:1-24.
62. Balla A., Kim Y.J., Varnai P., Szentpetery Z., Knight Z., Shokat K.M., et al. Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase III{alpha}. Mol. Biol. Cell 2008, 19:711-721.
63. Szentpetery Z., Varnai P., Balla T. Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc. Natl. Acad. Sci. USA 2010, 107:8225-8230.
64. Wong K.K., Engelman J.A., Cantley L.C. Targeting the PI3K signaling pathway in cancer. Curr. Opin. Genet. Dev. 2010, 20:87-90.
65. Walker D.H., Pike L.J. Phosphatidylinositol kinase is activated in membranes derived from cells treated with epidermal growth factor. Proc. Natl. Acad. Sci. USA 1987, 84:7513-7517.
66. Kauffmann-Zeh A., Thomas G.M., Ball A., Prosser S., Cunningham E., Cockcroft S., et al. Requirement for phosphatidylinositol transfer protein in epidermal growth factor signaling. Science 1995, 268:1188-1190.
67. Kauffmann-Zeh A., Klinger R., Endemann G., Waterfield M.D., Wetzker R., Hsuan J.J. Regulation of human type II phosphatidylinositol kinase activity by epidermal growth factor-dependent phosphorylation and receptor association. J. Biol. Chem. 1994, 269:31243-31251.
68. Cochet C., Filhol O., Payrastre B., Hunter T., Gill G.N. Interaction between the epidermal growth factor receptor and phosphoinositide kinases. J. Biol. Chem. 1991, 266:637-644.
69. Hammond G.R., Schiavo G., Irvine R.F. Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns (4,5)P(2). Biochem. J. 2009, 422:23-35.
70. Roesli C., Borgia B., Schliemann C., Gunthert M., Wunderli-Allenspach H., Giavazzi R., et al. Comparative analysis of the membrane proteome of closely related metastatic and nonmetastatic tumor cells. Cancer Res. 2009, 69:5406-5414.
71. Chuang Y.Y., Tran N.L., Rusk N., Nakada M., Berens M.E., Symons M. Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res. 2004, 64:8271-8275.
72. Chang-Ileto B., Frere S.G., Chan R.B., Voronov S.V., Roux A., Di Paolo G. Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev. Cell 2011, 20:206-218.
73. Chu K., Minogue S., Hsuan J., Waugh M. Differential effects of the phosphatidylinositol 4-kinases, PI4KIIalpha and PI4KIIIbeta, on Akt activation and apoptosis. Cell Death Dis. 2010, 1:e106. 10.1038/cddis.2010.84.
74. Wang Y.J., Wang J., Sun H.Q., Martinez M., Sun Y.X., Macia E., et al. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 2003, 114:299-310.
75. Waugh M.G., Minogue S., Blumenkrantz D., Anderson J.S., Hsuan J.J. Identification and characterization of differentially active pools of type IIalpha phosphatidylinositol 4-kinase activity in unstimulated A431 cells. Biochem. J. 2003, 376:497-503.
76. Li J., Lu Y., Zhang J., Kang H., Qin Z., Chen C., et al. PI4KIIalpha is a novel regulator of tumor growth by its action on angiogenesis and HIF-1alpha regulation. Oncogene 2010, 29:2550-2559.
77. Minogue S., Chu K.M., Westover E.J., Covey D.F., Hsuan J.J., Waugh M.G. Relationship between phosphatidylinositol 4-phosphate synthesis, membrane organization, and lateral diffusion of PI4KIIalpha at the trans- Golgi network. J. Lipid Res. 2010, 51:2314-2324.
78. Waugh M.G., Minogue S., Anderson J.S., Balinger A., Blumenkrantz D., Calnan D.P., et al. Localization of a highly active pool of type II phosphatidylinositol 4-kinase in a p97/valosin-containing-protein-rich fraction of the endoplasmic reticulum. Biochem. J. 2003, 373:57-63.
79. Begum N.A., Mori M., Matsumata T., Takenaka K., Sugimachi K., Barnard G.F. Differential display and integrin alpha 6 messenger RNA overexpression in hepatocellular carcinoma. Hepatology 1995, 22:1447-1455.
80. Torimura T., Ueno T., Kin M., Inuzuka S., Sugawara H., Tamaki S., et al. Coordinated expression of integrin alpha6beta1 and laminin in hepatocellular carcinoma. Hum. Pathol. 1997, 28:1131-1138.
81. Nejjari M., Hafdi Z., Dumortier J., Bringuier A.F., Feldmann G., Scoazec J.Y. Alpha6beta1 integrin expression in hepatocarcinoma cells: regulation and role in cell adhesion and migration. Int. J. Cancer 1999, 83:518-525.
82. Carloni V., Romanelli R.G., Mercurio A.M., Pinzani M., Laffi G., Cotrozzi G., Gentilini P. Knockout of alpha6 beta1-integrin expression reverses the transformed phenotype of hepatocarcinoma cell. Gastroenterology 1998, 115:433-442.
83. Carloni V., Mazzocca A., Pantaleo P., Cordella C., Laffi G., Gentilini P. The integrin, alpha6beta1, is necessary for the matrix-dependent activation of FAK and MAP kinase and the migration of human hepatocarcinoma cells. Hepatology 2001, 34:42-49.
84. Giannelli G., Bergamini C., Fransvea E., Sgarra C., Antonaci S. Laminin-5 with transforming growth factor-beta1 induces epithelial to mesenchymal transition in hepatocellular carcinoma. Gastroenterology 2005, 129:1375-1383.
85. Gerlinger M., Rowan A.J., Horswell S., Math M., Larkin J., Endesfelder D., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012, 366:883-892.