Tetraspanins in human epithelial malignancies

Journal of Pathology

Volumn 223, Issue 1, 2011, Pages 4-14

  Romanska, Hanna M ^a   Berditchevski, Fedor ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

biomarker; epithelial; human; tetraspanins; tumour

Indexed keywords

CD151 ANTIGEN; CD63 ANTIGEN; CD81 ANTIGEN; CD82 ANTIGEN; CD9 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TETRASPANIN; TETRASPANIN 1; TETRASPANIN 13; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR JUNB; UNCLASSIFIED DRUG; UROPLAKIN; UVOMORULIN;

ANTIGEN EXPRESSION; BLADDER CANCER; BREAST CANCER; CANCER GROWTH; CANCER RECURRENCE; CANCER STAGING; CANCER SURVIVAL; CARCINOGENESIS; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; COLORECTAL CANCER; EPITHELIUM TUMOR; GENE EXPRESSION; HEAD AND NECK CARCINOMA; HUMAN; LIVER CELL; MERKEL CELL TUMOR; METASTASIS; OVARY CANCER; OVERALL SURVIVAL; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CANCER; PROTEIN PROCESSING; REVIEW; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION REGULATION; VATER PAPILLA CARCINOMA;

ANTIGENS, CD; BREAST NEOPLASMS; FEMALE; HUMANS; KANGAI-1 PROTEIN; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; NEOPLASMS, GLANDULAR AND EPITHELIAL; TUMOR MARKERS, BIOLOGICAL;

EID: 78650023067     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2779     Document Type: Review

References (94)

1. Hemler ME,. Targeting of tetraspanin proteins-potential benefits and strategies. Nature Rev Drug Discov 2008; 7: 747-758.
2. Charrin S, le Naour F, Silvie O, et al., Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 2009; 420: 133-154.
3. Yanez-Mo M, Barreiro O, Gordon-Alonso M, et al., Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 2009; 19: 434-446.
4. Le Naour F, Zoller M,. The tumor antigen EpCAM: tetraspanins and the tight junction protein claudin-7, new partners, new functions. Front Biosci 2008; 13: 5847-5865.
5. Johnson JL, Winterwood N, DeMali KA, et al., Tetraspanin CD151 regulates RhoA activation and the dynamic stability of carcinoma cell-cell contacts. J Cell Sci 2009; 122: 2263-2273.
6. Novitskaya V, Romanska H, Dawoud M, et al., Tetraspanin CD151 regulates growth of mammary epithelial cells in three-dimensional extracellular matrix: implication for mammary ductal carcinoma in situ. Cancer Res; 70: 4698-4708.
7. Boucheix C, Duc GH, Jasmin C, et al., Tetraspanins and malignancy. Expert Rev Mol Med 2001; 2001: 1-17.
8. Wright MD, Moseley GW, van Spriel AB,. Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 2004; 64: 533-542.
9. Hemler ME,. Tetraspanin functions and associated microdomains. Nature Rev Mol Cell Biol 2005; 6: 801-811.
10. Tonoli H, Barrett JC,. CD82 metastasis suppressor gene: a potential target for new therapeutics? Trends Mol Med 2005; 11: 563-570.
11. Lazo PA,. Functional implications of tetraspanin proteins in cancer biology. Cancer Sci 2007; 98: 1666-1677.
12. Zoller M,. Tetraspanins: push and pull in suppressing and promoting metastasis. Nature Rev Cancer 2009; 9: 40-55.
13. Miyake M, Nakano K, Ieki Y, et al., Motility related protein 1 (MRP-1/CD9) expression: inverse correlation with metastases in breast cancer. Cancer Res 1995; 55: 4127-4131.
14. Miyake M, Nakano K, Itoi SI, et al., Motility-related protein-1 (MRP-1/CD9) reduction as a factor of poor prognosis in breast cancer. Cancer Res 1996; 56: 1244-1249.
15. Mimori K, Kataoka A, Yoshinaga K, et al., Identification of molecular markers for metastasis-related genes in primary breast cancer cells. Clin Exp Metastasis 2005; 22: 59-67.
16. Arihiro K, Kaneko M, Fujii S, et al., Loss of CD9 with expression of CD31 and VEGF in breast carcinoma, as predictive factors of lymph node metastasis. Breast Cancer 1998; 5: 131-138.
17. Jamil F, Peston D, Shousha S,. CD9 immunohistochemical staining of breast carcinoma: unlikely to provide useful prognostic information for routine use. Histopathology 2001; 39: 572-577.
18. Dong JT, Suzuki H, Pin SS, et al., Down-regulation of the KAI1 metastasis suppressor gene during the progression of human prostatic cancer infrequently involves gene mutation or allelic loss. Cancer Res 1996; 56: 4387-4390.
19. Yang X, Wei L, Tang C, et al., KAI1 protein is down-regulated during the progression of human breast cancer. Clin Cancer Res 2000; 6: 3424-3429.
20. Stark AM, Tongers K, Maass N, et al., Reduced metastasis-suppressor gene mRNA-expression in breast cancer brain metastases. J Cancer Res Clin Oncol 2005; 131: 191-198.
21. Christgen M, Bruchhardt H, Ballmaier M, et al., KAI1/CD82 is a novel target of estrogen receptor-mediated gene repression and downregulated in primary human breast cancer. Int J Cancer 2008; 123: 2239-2246.
22. Christgen M, Christgen H, Heil C, et al., Expression of KAI1/CD82 in distant metastases from estrogen receptor-negative breast cancer. Cancer Sci 2009; 100: 1767-1771.
23. Huang CI, Kohno N, Ogawa E, et al., Correlation of reduction in MRP-1/CD9 and KAI1/CD82 expression with recurrences in breast cancer patients. Am J Pathol 1998; 153: 973-983.
24. Yang XH, Richardson AL, Torres-Arzayus MI, et al., CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Res 2008; 68: 3204-3213.
25. Sadej R, Romanska H, Baldwin G, et al., CD151 regulates tumorigenesis by modulating the communication between tumor cells and endothelium. Mol Cancer Res 2009; 7: 787-798.
26. Huang H, Groth J, Sossey-Alaoui K, et al., Aberrant expression of novel and previously described cell membrane markers in human breast cancer cell lines and tumors. Clin Cancer Res 2005; 11: 4357-4364.
27. Wang JC, Begin LR, Berube NG, et al., Down-regulation of CD9 expression during prostate carcinoma progression is associated with CD9 mRNA modifications. Clin Cancer Res 2007; 13: 2354-2361.
28. Mori M, Mimori K, Shiraishi T, et al., Motility related protein 1 (MRP1/CD9) expression in colon cancer. Clin Cancer Res 1998; 4: 1507-1510.
29. Sho M, Adachi M, Taki T, et al., Transmembrane 4 superfamily as a prognostic factor in pancreatic cancer. Int J Cancer 1998; 79: 509-516.
30. Higashiyama M, Taki T, Ieki Y, et al., Reduced motility related protein-1 (MRP-1/CD9) gene expression as a factor of poor prognosis in non-small cell lung cancer. Cancer Res 1995; 55: 6040-6044.
31. Miyake M, Adachi M, Huang C, et al., A novel molecular staging protocol for non-small cell lung cancer. Oncogene 1999; 18: 2397-2404.
32. Kusukawa J, Ryu F, Kameyama T, et al., Reduced expression of CD9 in oral squamous cell carcinoma: CD9 expression inversely related to high prevalence of lymph node metastasis. J Oral Pathol Med 2001; 30: 73-79.
33. Erovic BM, Pammer J, Hollemann D, et al., Motility-related protein-1/CD9 expression in head and neck squamous cell carcinoma. Head Neck 2003; 25: 848-857. (Pubitemid 37139897)
34. Mhawech P, Dulguerov P, Tschanz E, et al., Motility-related protein-1 (MRP-1/CD9) expression can predict disease-free survival in patients with squamous cell carcinoma of the head and neck. Br J Cancer 2004; 90: 471-475.
35. Okochi H, Kato M, Nashiro K, et al., Expression of tetra-spans transmembrane family (CD9, CD37, CD53, CD63, CD81 and CD82) in normal and neoplastic human keratinocytes: an association of CD9 with alpha 3 beta 1 integrin. Br J Dermatol 1997; 137: 856-863.
36. Mhawech P, Herrmann F, Coassin M, et al., Motility-related protein 1 (MRP-1/CD9) expression in urothelial bladder carcinoma and its relation to tumor recurrence and progression. Cancer 2003; 98: 1649-1657.
37. Woegerbauer M, Thurnher D, Houben R, et al., Expression of the tetraspanins CD9, CD37, CD63, and CD151 in Merkel cell carcinoma: strong evidence for a posttranscriptional fine-tuning of CD9 gene expression. Mod Pathol 2010; 23: 751-762.
38. Sakamoto K, Nakamura Y, Nakashima T,. Immunohistochemical distribution of CD9 in parotid gland tumors. Auris Nasus Larynx 2004; 31: 49-55.
39. Gesierich S, Paret C, Hildebrand D, et al., Colocalization of the tetraspanins, CO-029 and CD151, with integrins in human pancreatic adenocarcinoma: impact on cell motility. Clin Cancer Res 2005; 11: 2840-2852.
40. Hori H, Yano S, Koufuji K, et al., CD9 expression in gastric cancer and its significance. J Surg Res 2004; 117: 208-215.
41. Soyuer S, Soyuer I, Unal D, et al., Prognostic significance of CD9 expression in locally advanced gastric cancer treated with surgery and adjuvant chemoradiotherapy. Pathol Res Pract 2010; 206: 607-610.
42. Murayama Y, Miyagawa J, Shinomura Y, et al., Significance of the association between heparin-binding epidermal growth factor-like growth factor and CD9 in human gastric cancer. Int J Cancer 2002; 98: 505-513.
43. Kuroda N, Inoue K, Guo L, et al., Expression of CD9/motility-related protein 1 (MRP-1) in renal parenchymal neoplasms: consistent expression in papillary and chromophobe renal cell carcinomas. Hum Pathol 2001; 32: 1071-1077.
44. Tozawa K, Akita H, Kawai N, et al., KAI1 expression can be a predictor of stage A prostate cancer progression. Prostate Cancer Prostatic Dis 2001; 4: 150-153.
45. Guo XZ, Friess H, Di Mola FF, et al., KAI1, a new metastasis suppressor gene, is reduced in metastatic hepatocellular carcinoma. Hepatology 1998; 28: 1481-1488.
46. Sun HC, Tang ZY, Zhou G, et al., KAI1 gene expression in hepatocellular carcinoma and its relationship with intrahepatic metastases. J Exp Clin Cancer Res 1998; 17: 307-311.
47. Lombardi DP, Geradts J, Foley JF, et al., Loss of KAI1 expression in the progression of colorectal cancer. Cancer Res 1999; 59: 5724-5731.
48. Maurer CA, Graber HU, Friess H, et al., Reduced expression of the metastasis suppressor gene KAI1 in advanced colon cancer and its metastases. Surgery 1999; 126: 869-880.
49. Wu DH, Liu L, Chen LH, et al., KAI1 gene expression in colonic carcinoma and its clinical significances. World J Gastroenterol 2004; 10: 2245-2249.
50. Hinoda Y, Adachi Y, Takaoka A, et al., Decreased expression of the metastasis suppressor gene KAI1 in gastric cancer. Cancer Lett 1998; 129: 229-234. (Pubitemid 28386606)
51. Wu Q, Ji Y, Zhang MQ, et al., Role of tumor metastasis suppressor gene KAI1 in digestive tract carcinomas and cancer cells. Cell Tissue Res 2003; 314: 237-249.
52. Tsutsumi S, Shimura T, Morinaga N, et al., Loss of KAI1 expression in gastric cancer. Hepatogastroenterology 2005; 52: 281-284. (Pubitemid 40282686)
53. Guo X, Friess H, Graber HU, et al., KAI1 expression is up-regulated in early pancreatic cancer and decreased in the presence of metastases. Cancer Res 1996; 56: 4876-4880.
54. Friess H, Guo XZ, Tempia-Caliera AA, et al., Differential expression of metastasis-associated genes in papilla of Vater and pancreatic cancer correlates with disease stage. J Clin Oncol 2001; 19: 2422-2432.
55. Liu FS, Dong JT, Chen JT, et al., Frequent down-regulation and lack of mutation of the KAI1 metastasis suppressor gene in epithelial ovarian carcinoma. Gynecol Oncol 2000; 78: 10-15.
56. Schindl M, Birner P, Breitenecker G, et al., Downregulation of KAI1 metastasis suppressor protein is associated with a dismal prognosis in epithelial ovarian cancer. Gynecol Oncol 2001; 83: 244-248.
57. Briese J, Schulte HM, Sajin M, et al., Correlations between reduced expression of the metastasis suppressor gene KAI-1 and accumulation of p53 in uterine carcinomas and sarcomas. Virchows Arch 2008; 453: 89-96.
58. Adachi M, Taki T, Ieki Y, et al., Correlation of KAI1/CD82 gene expression with good prognosis in patients with non-small cell lung cancer. Cancer Res 1996; 56: 1751-1755.
59. Adachi M, Taki T, Konishi T, et al., Novel staging protocol for non-small-cell lung cancers according to MRP-1/CD9 and KAI1/CD82 gene expression. J Clin Oncol 1998; 16: 1397-1406.
60. Chen Z, Mustafa T, Trojanowicz B, et al., CD82, and CD63 in thyroid cancer. Int J Mol Med 2004; 14: 517-527.
61. Geradts J, Maynard R, Birrer MJ, et al., Frequent loss of KAI1 expression in squamous and lymphoid neoplasms. An immunohistochemical study of archival tissues. Am J Pathol 1999; 154: 1665-1671.
62. Uzawa K, Ono K, Suzuki H, et al., High prevalence of decreased expression of KAI1 metastasis suppressor in human oral carcinogenesis. Clin Cancer Res 2002; 8: 828-835.
63. Imai Y, Sasaki T, Shinagawa Y, et al., Expression of metastasis suppressor gene (KAI1/CD82) in oral squamous cell carcinoma and its clinico-pathological significance. Oral Oncol 2002; 38: 557-561.
64. Farhadieh RD, Smee R, Ow K, et al., Down-regulation of KAI1/CD82 protein expression in oral cancer correlates with reduced disease free survival and overall patient survival. Cancer Lett 2004; 213: 91-98.
65. Uchida S, Shimada Y, Watanabe G, et al., Motility-related protein (MRP-1/CD9) and KAI1/CD82 expression inversely correlate with lymph node metastasis in oesophageal squamous cell carcinoma. Br J Cancer 1999; 79: 1168-1173.
66. Schindl M, Birner P, Bachtiary B, et al., The impact of expression of the metastasis suppressor protein KAI1 on prognosis in invasive squamous cell cervical cancer. Anticancer Res 2000; 20: 4551-4555.
67. Protzel C, Kakies C, Kleist B, et al., Down-regulation of the metastasis suppressor protein KAI1/CD82 correlates with occurrence of metastasis, prognosis and presence of HPV DNA in human penile squamous cell carcinoma. Virchows Arch 2008; 452: 369-375.
68. Yu Y, Yang JL, Markovic B, et al., Loss of KAI1 messenger RNA expression in both high-grade and invasive human bladder cancers. Clin Cancer Res 1997; 3: 1045-1049.
69. Su JS, Arima K, Hasegawa M, et al., Decreased expression of KAI1 metastasis suppressor gene is a recurrence predictor in primary pTa and pT1 urothelial bladder carcinoma. Int J Urol 2004; 11: 74-82.
70. Hashida H, Takabayashi A, Tokuhara T, et al., Clinical significance of transmembrane 4 superfamily in colon cancer. Br J Cancer 2003; 89: 158-167.
71. Houle CD, Ding XY, Foley JF, et al., Loss of expression and altered localization of KAI1 and CD9 protein are associated with epithelial ovarian cancer progression. Gynecol Oncol 2002; 86: 69-78.
72. Hashida H, Takabayashi A, Tokuhara T, et al., Integrin alpha3 expression as a prognostic factor in colon cancer: association with MRP-1/CD9 and KAI1/CD82. Int J Cancer 2002; 97: 518-525.
73. Ang J, Lijovic M, Ashman LK, et al., 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; 13: 1717-1721.
74. Ke AW, Shi GM, Zhou J, et al., Role of overexpression of CD151 and/or c-Met in predicting prognosis of hepatocellular carcinoma. Hepatology 2009; 49: 491-503.
75. Tokuhara T, Hasegawa H, Hattori N, et al., Clinical significance of CD151 gene expression in non-small cell lung cancer. Clin Cancer Res 2001; 7: 4109-4114.
76. Chien CW, Lin SC, Lai YY, et al., Regulation of CD151 by hypoxia controls cell adhesion and metastasis in colorectal cancer. Clin Cancer Res 2008; 14: 8043-8051.
77. Chen L, Wang Z, Zhan X, et al., Association of NET-1 gene expression with human hepatocellular carcinoma. Int J Surg Pathol 2007; 15: 346-353. (Pubitemid 47476082)
78. Scholz CJ, Kurzeder C, Koretz K, et al., Tspan-1 is a tetraspanin preferentially expressed by mucinous and endometrioid subtypes of human ovarian carcinomas. Cancer Lett 2009; 275: 198-203.
79. Kanetaka K, Sakamoto M, Yamamoto Y, et al., Overexpression of tetraspanin CO-029 in hepatocellular carcinoma. J Hepatol 2001; 35: 637-642.
80. Kuhn S, Koch M, Nubel T, et al., A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol Cancer Res 2007; 5: 553-567.
81. Zhou Z, Ran YL, Hu H, et al., TM4SF3 promotes esophageal carcinoma metastasis via upregulating ADAM12m expression. Clin Exp Metastasis 2008; 25: 537-548.
82. Arencibia JM, Martin S, Perez-Rodriguez FJ, et al., Gene expression profiling reveals overexpression of TSPAN13 in prostate cancer. Int J Oncol 2009; 34: 457-463.
83. Kageyama S, Yoshiki T, Isono T, et al., High expression of human uroplakin Ia in urinary bladder transitional cell carcinoma. Jpn J Cancer Res 2002; 93: 523-531.
84. Lopez-Beltran A, Montironi R, Blanca A, et al., Invasive micropapillary urothelial carcinoma of the bladder. Hum Pathol; 41: 1159-1164.
85. Olsburgh J, Harnden P, Weeks R, et al., Uroplakin gene expression in normal human tissues and locally advanced bladder cancer. J Pathol 2003; 199: 41-49.
86. Inoue G, Horiike N, Onji M,. The CD81 expression in liver in hepatocellular carcinoma. Int J Mol Med 2001; 7: 67-71.
87. Mashimo T, Watabe M, Hirota S, et al., The expression of the KAI1 gene, a tumor metastasis suppressor, is directly activated by p53. Proc Natl Acad Sci U S A 1998; 95: 11307-11311.
88. Shinohara T, Nishimura N, Hanibuchi M, et al., Transduction of KAI1/CD82 cDNA promotes hematogenous spread of human lung-cancer cells in natural killer cell-depleted SCID mice. Int J Cancer 2001; 94: 16-23.
89. Marreiros A, Dudgeon K, Dao V, et al., KAI1 promoter activity is dependent on p53, junB and AP2: evidence for a possible mechanism underlying loss of KAI1 expression in cancer cells. Oncogene 2005; 24: 637-649.
90. Guo C, Liu QG, Zhang L, et al., Expression and clinical significance of p53, JunB and KAI1/CD82 in human hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 2009; 8: 389-396.
91. Kim JH, Kim B, Cai L, et al., Transcriptional regulation of a metastasis suppressor gene by Tip60 and beta-catenin complexes. Nature 2005; 434: 921-926.
92. Wang J, Liu X, Ni P, et al., SP1 is required for basal activation and chromatin accessibility of CD151 promoter in liver cancer cells. Biochem Biophys Res Commun 2010; 393: 291-296.
93. Tsai YC, Mendoza A, Mariano JM, et al., The ubiquitin ligase gp78 promotes sarcoma metastasis by targeting KAI1 for degradation. Nature Med 2007; 13: 1504-1509.
94. Lineberry N, Su L, Soares L, et al., The single subunit transmembrane E3 ligase gene related to anergy in lymphocytes (GRAIL) captures and then ubiquitinates transmembrane proteins across the cell membrane. J Biol Chem 2008; 283: 28497-28505.