CD44v/CD44s expression patterns are associated with the survival of pancreatic carcinoma patients

Diagnostic Pathology

Volumn 9, Issue 1, 2014, Pages

  Li, Zhonghu ^a   Chen, Kai ^a   Jiang, Peng ^a   Zhang, Xi ^a   Li, Xiaowu ^a   Li, Zhihua ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

CD44; CD44s; CD44v; Pancreatic carcinoma; Survival

Indexed keywords

CD44 PROTEIN, HUMAN; CD44S ANTIGEN; CD44V10 ANTIGEN; HERMES ANTIGEN; TUMOR MARKER;

AGED; CANCER STAGING; CARCINOMA; CHI SQUARE DISTRIBUTION; DISEASE COURSE; FEMALE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HUMAN; IMMUNOLOGY; KAPLAN MEIER METHOD; MALE; MIDDLE AGED; MORTALITY; MULTIVARIATE ANALYSIS; PANCREAS TUMOR; PATHOLOGY; PROPORTIONAL HAZARDS MODEL; RISK FACTOR; SECONDARY; TIME; TUMOR CELL LINE;

AGED; ANTIGENS, CD44; CARCINOMA; CELL LINE, TUMOR; CHI-SQUARE DISTRIBUTION; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VARIATION; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM STAGING; PANCREATIC NEOPLASMS; PROPORTIONAL HAZARDS MODELS; RISK FACTORS; TIME FACTORS; TUMOR MARKERS, BIOLOGICAL;

EID: 84900036986     PISSN: None     EISSN: 17461596     Source Type: Journal    
DOI: 10.1186/1746-1596-9-79     Document Type: Article

References (56)

1. Abel EV, Simeone DM. Biology and clinical applications of pancreatic cancer stem cells. Gastroenterology 2013, 144:1241-1248. 10.1053/j.gastro.2013.01.072, 23622133.
2. Wolfgang CL, Herman JM, Laheru DA, Klein AP, Erdek MA, Fishman EK, Hruban RH. Recent progress in pancreatic cancer. CA Cancer J Clin 2013, 63:318-348. 10.3322/caac.21190, 23856911.
3. Maeda S, Shinchi H, Kurahara H, Mataki Y, Noma H, Maemura K, Aridome K, Yokomine T, Natsugoe S, Aikou T, Takao S. Clinical significance of midkine expression in pancreatic head carcinoma. Br J Cancer 2007, 97:405-411. 10.1038/sj.bjc.6603879, 2360321, 17622248.
4. Goldstein LA, Zhou DF, Picker LJ, Minty CN, Bargatze RF, Ding JF, Butcher EC. A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins. Cell 1989, 56:1063-1072. 10.1016/0092-8674(89)90639-9, 2466576.
5. Stamenkovic I, Amiot M, Pesando JM, Seed B. A lymphocyte molecule implicated in lymph node homing is a member of the cartilage link protein family. Cell 1989, 56:1057-1062. 10.1016/0092-8674(89)90638-7, 2466575.
6. Screaton GR, Bell MV, Bell JI, Jackson DG. The identification of a new alternative exon with highly restricted tissue expression in transcripts encoding the mouse Pgp-1 (CD44) homing receptor. Comparison of all 10 variable exons between mouse, human, and rat. J Biol Chem 1993, 268:12235-12238.
7. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U, Bell JI. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci U S A 1992, 89:12160-12164. 10.1073/pnas.89.24.12160, 50718, 1465456.
8. Tolg C, Hofmann M, Herrlich P, Ponta H. Splicing choice from ten variant exons establishes CD44 variability. Nucleic Acids Res 1993, 21:1225-1229. 10.1093/nar/21.5.1225, 309286, 8464707.
9. Gallatin WM, Weissman IL, Butcher EC. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 1983, 304:30-34. 10.1038/304030a0, 6866086.
10. Haegel H, Dierich A, Ceredig R. CD44 in differentiated embryonic stem cells: surface expression and transcripts encoding multiple variants. Dev Immunol 1994, 3:239-246. 10.1155/1994/25484, 2275938, 7542511.
11. Du L, Wang H, He L, Zhang J, Ni B, Wang X, Jin H, Cahuzac N, Mehrpour M, Lu Y, Chen Q. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res 2008, 14:6751-6760. 10.1158/1078-0432.CCR-08-1034, 18980968.
12. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005, 65:5506-5511. 10.1158/0008-5472.CAN-05-0626, 15994920.
13. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly JG, Chandra D, Zhou J, Claypool K. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006, 25:1696-1708. 10.1038/sj.onc.1209327, 16449977.
14. Haynes BF, Liao HX, Patton KL. The transmembrane hyaluronate receptor (CD44): multiple functions, multiple forms. Cancer Cells 1991, 3:347-350.
15. Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, Watanabe M, Beppu T, Tamada M, Nagano O. CD44s regulates the TGF-beta-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res 2012, 72:3414-3423. 10.1158/0008-5472.CAN-12-0299, 22552294.
16. Ryu HS, Park SH, Lee KB, Shin E, Jang JJ. Expression of the Transmembrane Glycoprotein CD44s Is Potentially an Independent Predictor of Recurrence in Hepatocellular Carcinoma. Gut Liver 2011, 5:204-209. 10.5009/gnl.2011.5.2.204, 3140667, 21814602.
17. Zhang J, Chang B, Liu J. CD44 standard form expression is correlated with high-grade and advanced-stage ovarian carcinoma but not prognosis. Hum Pathol 2013, 44:1882-1889. 10.1016/j.humpath.2013.02.016, 23664487.
18. Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, Cheng C. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Invest 2011, 121:1064-1074. 10.1172/JCI44540, 3049398, 21393860.
19. Afify AM, Tate S, Durbin-Johnson B, Rocke DM, Konia T. Expression of CD44s and CD44v6 in lung cancer and their correlation with prognostic factors. Int J Biol Markers 2011, 26:50-57. 10.5301/JBM.2011.6291, 21279958.
20. Costa WH, Rocha RM, Cunha IW, Guimaraes GC, Zequi Sde C. Immunohistochemical expression of CD44s in renal cell carcinoma lacks independent prognostic significance. Int Braz J Urol 2012, 38:456-465. 10.1590/S1677-55382012000400004, 22951174.
21. Dome B, Somlai B, Ladanyi A, Fazekas K, Zoller M, Timar J. Expression of CD44v3 splice variant is associated with the visceral metastatic phenotype of human melanoma. Arch: Int J Oral Maxillofac Pathol 2001, 439:628-635.
22. Sun BS, Li Y, Zhang ZF, You J, Wang CL. Osteopontin combined With CD44v6, a novel prognostic biomarker in non-small cell lung cancer undergoing curative resection. Ann Thorac Surg 2013, 96:1943-1951. 10.1016/j.athoracsur.2013.07.089, 24094519.
23. Shi J, Zhou Z, Di W, Li N. Correlation of CD44v6 expression with ovarian cancer progression and recurrence. BMC Cancer 2013, 13:182. 10.1186/1471-2407-13-182, 3635997, 23565736.
24. Saito S, Okabe H, Watanabe M, Ishimoto T, Iwatsuki M, Baba Y, Tanaka Y, Kurashige J, Miyamoto Y, Baba H. CD44v6 expression is related to mesenchymal phenotype and poor prognosis in patients with colorectal cancer. Oncol Rep 2013, 29:1570-1578.
25. Li XD, Ji M, Wu J, Jiang JT, Wu CP. Clinical significance of CD44 variants expression in colorectal cancer. Tumori 2013, 99:88-92.
26. Hsieh HF, Yu JC, Ho LI, Chiu SC, Harn HJ. Molecular studies into the role of CD44 variants in metastasis in gastric cancer. Mol Pathol 1999, 52:25-28. 10.1136/mp.52.1.25, 395666, 10439835.
27. Gotte M, Yip GW. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res 2006, 66:10233-10237. 10.1158/0008-5472.CAN-06-1464, 17079438.
28. Takahashi K. Restoration of CD44S in non-small cell lung cancer cells enhanced their susceptibility to the macrophage cytotoxicity. Lung Cancer 2003, 41:145-153. 10.1016/S0169-5002(03)00224-1, 12871777.
29. Montgomery E, Abraham SC, Fisher C, Deasel MR, Amr SS, Sheikh SS, House M, Lilliemoe K, Choti M, Brock M. CD44 loss in gastric stromal tumors as a prognostic marker. Am J Surg Pathol 2004, 28:168-177. 10.1097/00000478-200402000-00003, 15043305.
30. Lazari P, Poulias H, Gakiopoulou H, Thomopoulou GH, Barbatis C, Lazaris AC. Differential immunohistochemical expression of CD44s, E-cadherin and beta-catenin among hyperplastic and neoplastic lesions of the prostate gland. Urol Int 2013, 90:109-116. 10.1159/000345057, 23220849.
31. Gunia S, May M, Koch S, Dietel M, Erbersdobler A. Expression of CD44s in incidental prostate cancer is more strongly associated with Gleason scores on subsequent radical prostatectomies than conventional prognostic parameters. Pathobiology 2009, 76:286-292. 10.1159/000245894, 19955840.
32. Kuo KT, Liang CW, Hsiao CH, Lin CH, Chen CA, Sheu BC, Lin MC. Downregulation of BRG-1 repressed expression of CD44s in cervical neuroendocrine carcinoma and adenocarcinoma. Mod Pathol 2006, 19:1570-1577. 10.1038/modpathol.3800687, 16998464.
33. Jeffrey S, Ross M. Decreased CD44 standard form expression correlates with prognostic variables in ovarian carcinomas. Am J Clin Pathol 2001, 116:122-128. 10.1309/KUK0-1M3D-LGNE-THXR, 11447742.
34. Pacifico MD, Grover R, Richman PI, Daley FM, Buffa F, Wilson GD. CD44v3 levels in primary cutaneous melanoma are predictive of prognosis: assessment by the use of tissue microarray. Int J Cancer 2006, 118:1460-1464. 10.1002/ijc.21504, 16187282.
35. Yamada Y, Itano N, Narimatsu H, Kudo T, Hirohashi S, Ochiai A, Tohnai I, Ueda M, Kimata K. CD44 variant exon 6 expressions in colon cancer assessed by quantitative analysis using real time reverse transcriptase-polymerase chain reaction. Oncol Rep 2003, 10:1919-1924.
36. Zalewski B. Levels of v5 and v6 CD44 splice variants in serum of patients with colorectal cancer are not correlated with pT stage, histopathological grade of malignancy and clinical features. World J Gastroenterol 2004, 10:583-585.
37. Diaz LK, Zhou X, Wright ET, Cristofanilli M, Smith T, Yang Y, Sneige N, Sahin A, Gilcrease MZ. CD44 expression is associated with increased survival in node-negative invasive breast carcinoma. Clin Cancer Res 2005, 11:3309-3314. 10.1158/1078-0432.CCR-04-2184, 15867228.
38. Foekens JA, Dall P, Klijn JG, Skroch-Angel P, Claassen CJ, Look MP, Ponta H, Van Putten WL, Herrlich P, Henzen-Logmans SC. Prognostic value of CD44 variant expression in primary breast cancer. Int J Cancer 1999, 84:209-215. 10.1002/(SICI)1097-0215(19990621)84:3<209::AID-IJC2>3.0.CO;2-9, 10371335.
39. Friedrichs K, Franke F, Lisboa BW, Kugler G, Gille I, Terpe HJ, Holzel F, Maass H, Gunthert U. CD44 isoforms correlate with cellular differentiation but not with prognosis in human breast cancer. Cancer Res 1995, 55:5424-5433.
40. Tsukuda H, Matsumura Y, Inoue T, Kobayashi Y, Ookawa K, Aoki T, Nebiki H, Yamazaki O, Kondo H, Kakizoe T. Diagnostic application of CD44 variant expression in pancreatic juice for detection of pancreatic neoplasm. Anticancer Res 2001, 21:2175-2183.
41. Rall CJ, Rustgi AK. CD44 isoform expression in primary and metastatic pancreatic adenocarcinoma. Cancer Res 1995, 55:1831-1835.
42. Tomaszewska R. [Morphologic, morphometric and immunohistochemical studies on pancreatic intraductal hyperplasia and infiltrating carcinoma]. Folia Med Cracov 1999, 40:101-141.
43. Gotoda T, Matsumura Y, Kondo H, Saitoh D, Shimada Y, Kosuge T, Kanai Y, Kakizoe T. Expression of CD44 variants and its association with survival in pancreatic cancer. Jpn J Cancer Res 1998, 89:1033-1040. 10.1111/j.1349-7006.1998.tb00493.x, 9849582.
44. Konig H, Moll J, Ponta H, Herrlich P. Trans-acting factors regulate the expression of CD44 splice variants. EMBO J 1996, 15:4030-4039. 452123, 8670907.
45. Slominski AT, Raso-Barnett L, Banky B, Barbai T, Becsagh P, Timar J, Raso E. Demonstration of a melanoma-specific CD44 alternative splicing pattern that remains qualitatively stable, but shows quantitative changes during tumour progression. PLoS One 2013, 8:e53883. 10.1371/journal.pone.0053883, 3544768, 23342032.
46. Sullu Y, Gun S, Atmaca S, Karagoz F, Kandemir B. Poor prognostic clinicopathologic features correlate with VEGF expression but not with PTEN expression in squamous cell carcinoma of the larynx. Diagn Pathol 2010, 5:35. 10.1186/1746-1596-5-35, 2904738, 20546613.
47. Zhou G, Chiu D, Qin D, Niu L, Cai J, He L, Tan D, Xu K. Expression of CD44v6 and integrin-beta1 for the prognosis evaluation of pancreatic cancer patients after cryosurgery. Diagn Pathol 2013, 8:146. 10.1186/1746-1596-8-146, 3846138, 24004467.
48. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011, 19:387-400. 10.1016/j.ccr.2011.01.038, 21397861.
49. Abetamann V, Kern HF, Elsasser HP. Differential expression of the hyaluronan receptors CD44 and RHAMM in human pancreatic cancer cells. Clin Cancer Res 1996, 2:1607-1618.
50. Yasui W, Kudo Y, Naka K, Fujimoto J, Ue T, Yokozaki H, Tahara E. Expression of CD44 containing variant exon 9 (CD44v9) in gastric adenomas and adenocarcinomas: relation to the proliferation and progression. Int J Oncol 1998, 12:1253-1258.
51. Ue T, Yokozaki H, Kitadai Y, Yamamoto S, Yasui W, Ishikawa T, Tahara E. Co-expression of osteopontin and CD44v9 in gastric cancer. Int J Cancer 1998, 79:127-132. 10.1002/(SICI)1097-0215(19980417)79:2<127::AID-IJC5>3.0.CO;2-V, 9583725.
52. Omara-Opyene AL, Qiu J, Shah GV, Iczkowski KA. Prostate cancer invasion is influenced more by expression of a CD44 isoform including variant 9 than by Muc18. Lab Invest 2004, 84:894-907. 10.1038/labinvest.3700112, 15107804.
53. Goi T, Koneri K, Katayama K, Hirose K, Yamaguchi A. Evaluation of clinicopathological factors and the correlation between the adhesion molecule CD44 variant 9 expression and pulmonary metastases from colorectal cancers. Int Surg 2002, 87:130-136.
54. Afify A, McNiel MA, Braggin J, Bailey H, Paulino AF. Expression of CD44s, CD44v6, and hyaluronan across the spectrum of normal-hyperplasia-carcinoma in breast. Appl Immunohistochem Mol Morphol 2008, 16:121-127. 10.1097/PAI.0b013e318047df6d, 18227732.
55. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P, Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 2002, 16:3074-3086. 10.1101/gad.242602, 187488, 12464636.
56. Mielgo A, van Driel M, Bloem A, Landmann L, Gunthert U. A novel antiapoptotic mechanism based on interference of Fas signaling by CD44 variant isoforms. Cell Death Differ 2006, 13:465-477. 10.1038/sj.cdd.4401763, 16167069.