De novo expression of CD44 variants in sporadic and hereditary gastric cancer

Laboratory Investigation

Volumn 90, Issue 11, 2010, Pages 1604-1614

  Da Cunha, Cristiana Branco ^a,b   Oliveira, Carla ^a,c   Wen, Xiaogang ^a,d   Gomes, Bárbara ^a,d   Sousa, Sónia ^a   Suriano, Gianpaolo ^a,c   Grellier, Maritie ^a   Huntsman, David G ^e,f   Carneiro, Fátima ^a,c,d   Granja, Pedro L ^a,b   Seruca, Raquel ^a,c  

^a UNIVERSITY OF PORTO   (Portugal)

^b INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

^c University of Porto   (Portugal)

^d HOSPITAL DE SÃO JOÃO   (Portugal)

^e BRITISH COLUMBIA CANCER AGENCY   (Canada)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

CD44; CD44v6; E cadherin; HDGC; splicing; sporadic GC

Indexed keywords

CD44V6 ANTIGEN; CD44V7 ANTIGEN; HERMES ANTIGEN; MESSENGER RNA; TUMOR MARKER; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FAMILIAL CANCER; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTESTINE METAPLASIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; STOMACH; STOMACH CANCER; STOMACH MUCOSA; STOMACH POLYP;

EID: 78049336816     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2010.155     Document Type: Article

References (60)

1. Aruffo A, Stamenkovic I, Melnick M, et al. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990;61:1303-1313.
2. Screaton GR, Bell MV, Jackson DG, et al. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci USA 1992;89: 12160-12164.
3. Ponta H, Wainwright D, Herrlich P. Molecules in focus The CD44 protein family. Int J Biochem Cell Biol 1998;30:299-305.
4. Rudzki Z, Jothy S. CD44 and the adhesion of neoplastic cells. Mol Pathol 1997;50:57-71.
5. Shtivelman E, Bishop JM. Expression of CD44 is repressed in neuroblastoma cells. Mol Cell Biol 1991;11:5446-5453.
6. De Marzo AM, Bradshaw C, Sauvageot J, et al. CD44 and CD44v6 downregulation in clinical prostatic carcinoma: relation to Gleason grade and cytoarchitecture. Prostate 1998;34:162-168.
7. Joensuu H, Klemi PJ, Toikkanen S, et al. Glycoprotein CD44 expression and its association with survival in breast cancer. Am J Pathol 1993;143:867-874.
8. Friedrichs K, Kugler G, Franke F, et al. CD44 isoforms in prognosis of breast cancer. Lancet 1995;345:1237.
9. Kaufmann M, Heider KH, Sinn HP, et al. CD44 variant exon epitopes in primary breast cancer and length of survival. Lancet 1995;345:615-619.
10. Mulder JW, Kruyt PM, Sewnath M, et al. Colorectal cancer prognosis and expression of exon-v6-containing CD44 proteins. Lancet 1994;344: 1470-1472.
11. Wielenga VJ, Heider KH, Offerhaus GJ, et al. Expression of CD44 variant proteins in human colorectal cancer is related to tumor progression. Cancer Res 1993;53:4754-4756.
12. Terpe HJ, Koopmann R, Imhof BA, et al. Expression of integrins and CD44 isoforms in non-Hodgkin's lymphomas: CD44 variant isoforms are preferentially expressed in high-grade malignant lymphomas. J Pathol 1994;174:89-100.
13. Takaishi S, Okumura T, Tu S, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009;27: 1006-1020.
14. Heider K-H, Dammrich J, Skroch-Angel P, et al. Differential EXpression of CD44 splice variants in intestinal-and diffuse-type human gastric carcinomas and normal gastric mucosa. Cancer Res 1993;53: 4197-4203.
15. Mayer B, Jauch KW, Gunthert U, et al. De-novo expression of CD44 and survival in gastric cancer. Lancet 1993;342:1019-1022.
16. Muller W, Schneiders A, Heider KH, et al. Expression and prognostic value of the CD44 splicing variants v5 and v6 in gastric cancer. J Pathol 1997;183:222-227.
17. Mirecka J, Marx D, Schauer A. Immunohistochemical localization of CD44 variants 5 and 6 in human gastric mucosa and gastric cancer. Anticancer Res 1995;15:1459-1465.
18. Heider KH, Dammrich J, Skroch-Angel P, et al. Differential expression of CD44 splice variants in intestinal-and diffuse-type human gastric carcinomas and normal gastric mucosa. Cancer Res 1993;53: 4197-4203.
19. Hong RL, Lee WJ, Shun CT, et al. Expression of CD44 and its clinical implication in diffuse-type and intestinal-type gastric adenocarcinomas. Oncology 1995;52:334-339.
20. Ghaffarzadehgan K, Jafarzadeh M, Raziee HR, et al. Expression of cell adhesion molecule CD44 in gastric adenocarcinoma and its prognostic importance. World J Gastroenterol 2008;14:6376-6381.
21. Carneiro F, Huntsman DG, Smyrk TC, et al. Model of the early development of diffuse gastric cancer in E-cadherin mutation carriers and its implications for patient screening. J Pathol 2004;203: 681-687.
22. Suriano G, Mulholland D, de Wever O, et al. The intracellular E-cadherin germline mutation V832M lacks the ability to mediate cell-cell adhesion and to suppress invasion. Oncogene 2003;22:5716-5719.
23. Suriano G, Oliveira C, Ferreira P, et al. Identification of CDH1 germline missense mutations associated with functional inactivation of the E-cadherin protein in young gastric cancer probands. Hum Mol Genet 2003;12:575-582.
24. Suriano G, Oliveira MJ, Huntsman D, et al. E-cadherin germline missense mutations and cell phenotype: evidence for the independence of cell invasion on the motile capabilities of the cells. Hum Mol Genet 2003;12:3007-3016.
25. Oliveira C, Bordin MC, Grehan N, et al. Screening E-cadherin in gastric cancer families reveals germline mutations only in hereditary diffuse gastric cancer kindred. Hum Mutat 2002;19:510-517.
26. Machado JC, Oliveira C, Carvalho R, et al. E-cadherin gene (CDH1) promoter methylation as the second hit in sporadic diffuse gastric carcinoma. Oncogene 2001;20:1525-1528.
27. Huntsman DG, Carneiro F, Lewis FR, et al. Early gastric cancer in young, asymptomatic carriers of germ-line E-cadherin mutations. N Engl J Med 2001;344:1904-1909.
28. Carneiro F, Machado JC, Seruca R, et al. E-cadherin changes in gastric carcimona. Histopathology 1999;35:477-478.
29. Mateus AR, Simoes-Correia J, Figueiredo J, et al. E-cadherin mutations and cell motility: a genotype-phenotype correlation. Exp Cell Res 2009;315:1393-1402.
30. Oliveira C, Senz J, Kaurah P, et al. Germline CDH1 deletions in hereditary diffuse gastric cancer families. Hum Mol Genet 2009;18:1545-1555.
31. Oliveira C, Sousa S, Pinheiro H, et al. Quantification of epigenetic and genetic second hits in CDH1 during hereditary diffuse gastric cancer syndrome progression. Gastroenterology 2009;136:2137-2148.
32. Lynch HT, Grady W, Suriano G, et al. Gastric cancer: new genetic developments. J Surg Oncol 2005;90:114-133; discussion 133.
33. Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 1965;64:31-49.
34. Filipe MI, Jass JR. Intestinal metaplasia subtypes and cancer risk. In: Gastric Carcinoma.Filipe MI, Jass JR (eds). Churchill Livingstone: London, 1986, pp 87-115.
35. Sato S, Yokozaki H, Yasui W, et al. Silencing of the CD44 gene by CpG methylation in a human gastric carcinoma cell line. Jpn J Cancer Res 1999;90:485-489.
36. Guilford P HJ, Harraway J, McLeod M, et al. E-cadherin germline mutations in familial gastric cancer. Nature 1998;26:6674.
37. Günthert U, Hofmann M, Rudy W, et al. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 1991; 65:13-24.
38. Orian-Rousseau Vr, Chen L, Sleeman JP, et al. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 2002;16:3074-3086.
39. Damm SPK, Stefan M, Wels C, et al. HGF-Promoted Motility in Primary Melanocytes Depends on CD44v6 Regulated via NF-kappa B, Egr-1, and C/EBP-beta. J Investig Dermatol 2010;130:1893-1903.
40. Mielgo A, van Driel M, Bloem A, et al. A novel antiapoptotic mechanism based on interference of Fas signaling by CD44 variant isoforms. Cell Death Differ 2006;13:465-477.
41. Marhaba R, Bourouba M, Zoller M. CD44v6 promotes proliferation by persisting activation of MAP kinases. Cell Signal 2005;17:961-973.
42. Bates RC, Edwards NS, Burns GF, et al. A CD44 survival pathway triggers chemoresistance via lyn kinase and phosphoinositide 3-kinase/Akt in colon carcinoma cells. Cancer Res 2001;61:5275-5283.
43. Carvalho R, Milne AN, Polak M, et al. A novel region of amplification at 11p12-13 in gastric cancer, revealed by representational difference analysis, is associated with overexpression of CD44v6, especially in early-onset gastric carcinomas. Genes Chromosomes Cancer 2006;45: 967-975.
44. Heider KH, Hofmann M, Hors E, et al. A human homologue of the rat metastasis-associated variant of CD44 is expressed in colorectal carcinomas and adenomatous polyps. J Cell Biol 1993;120:227-233.
45. Gulmann C, Grace A, Leader M, et al. CD44v6: a potential marker of malignant transformation in intestinal metaplasia of the stomach? An immunohistochemical study using tissue microarrays. Eur J Gastroenterol Hepatol 2003;15:981-986.
46. Wimmel A, Kogan E, Ramaswamy A, et al. Variant expression of CD44 in preneoplastic lesions of the lung. Cancer 2001;92:1231-1236.
47. Afify AM, Craig S, Paulino AF, et al. Expression of hyaluronic acid and its receptors, CD44s and CD44v6, in normal, hyperplastic, and neoplastic endometrium. Ann Diagn Pathol 2005;9:312-318.
48. Soon Cheol H, Jae Yun S, Jae Kwan L, et al. Significance of CD44v6 expression in gynecologic malignancies. J Obstet Gynaecol Res 2006;32:379-386.
49. Afify A, McNiel MA, Braggin J, et al. Expression of CD44s, CD44v6, and hyaluronan across the spectrum of normal-hyperplasia-carcinoma in breast. Appl Immunohistochem Mol Morphol 2008;16:121-127.
50. Judd LM, Andriga A, Rubio CA, et al. Gastric achlorhydria in H/K-ATPase-deficient (Atp4a(-/-)) mice causes severe hyperplasia, muco-cystic metaplasia and upregulation of growth factors. J Gastroenterol Hepatol 2005;20:1266-1278.
51. Liu YJ, Yan PS, Li J, et al. Expression and significance of CD44 s, CD44v6, and nm23 mRNA in human cancer. World J Gastroenterol 2005;11: 6601-6606.
52. Polkowski WP, Skomra DG, Mielko J, et al. E-cadherin expression as predictive marker of proximal resection line involvement for advanced carcinoma of the gastric cardia. E J Surg Oncol 2004;30:1084-1092.
53. Seiter S AR, Reber S, Komitowski D, et al. Prevention of tumor metastasis formation by anti-variant CD44. J Experiment Med 1993; 177:443-455.
54. Reeder JA, Gotley DC, Walsh MD, et al. Expression of ANTisense CD44 variant 6 inhibits colorectal tumor metastasis and tumor growth in a wound environment. Cancer Res 1998;58:3719-3726.
55. Nishii T, Yashiro M, Shinto O, et al. Cancer stem cell-like SP cells have a high adhesion ability to the peritoneum in gastric carcinoma. Cancer Sci 2009;100:1397-1402.
56. Carneiro F, Huntsman DG, Smyrk TC, et al. Model of the early development of diffuse gastric cancer in E-cadherin mutation carriers and its implications for patient screening. J Pathol 2004;203:681-687.
57. Pharoah PDP, Guilford P, Caldas C. The International Gastric Cancer Linkage C. Incidence of gastric cancer and breast cancer in CDH1 (E-cadherin) mutation carriers from hereditary diffuse gastric cancer families. Gastroenterology 2001;121:1348-1353.
58. Humar B, Fukuzawa R, Blair V, et al. Destabilized adhesion in the gastric proliferative zone and c-Src kinase activation mark the development of early diffuse gastric cancer. Cancer Res 2007;67:2480-2489.
59. Ferrari M. Cancer Nanotechnology: opportunities and challenges. Nat Rev Cancer 2005;5:161-171.
60. Wu YWW, Chen Y, Huang K, et al. The investigation of polymer-siRNA nanoparticle for gene therapy of gastric cancer in vitro. Int J Nanomed 2010;5:129-136.