Podoplanin expression in cancerous stroma induces lymphangiogenesis and predicts lymphatic spread and patient survival

Archives of Pathology and Laboratory Medicine

Volumn 134, Issue 10, 2010, Pages 1520-1527

  Kitano, Haruhisa ^a,b   Kageyama, Shun Ichiro ^a   Hewitt, Stephen M ^c   Hayashi, Ryuji ^d   Doki, Yoshinori ^d   Ozaki, Yoshitomo ^a,b   Fujino, Shozo ^a,b   Takikita, Mikiko ^c   Kubo, Hajime ^e   Fukuoka, Junya ^a  

^a TOYAMA UNIVERSITY HOSPITAL   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF TOYAMA   (Japan)

^e KYOTO UNIVERSITY HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN;

ADENOCARCINOMA; AGE; ARTICLE; CANCER INVASION; CANCER STAGING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG NON SMALL CELL CANCER; LUNG TUMOR; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; MALE; METHODOLOGY; MORTALITY; OVARY TUMOR; PATHOLOGY; PREDICTION AND FORECASTING; PROGNOSIS; PROSTATE TUMOR; PROTEIN MICROARRAY; STROMA CELL; SURVIVAL RATE;

ADENOCARCINOMA; AGE FACTORS; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; MALE; MEMBRANE GLYCOPROTEINS; NEOPLASM INVASIVENESS; NEOPLASM STAGING; OVARIAN NEOPLASMS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROSTATIC NEOPLASMS; PROTEIN ARRAY ANALYSIS; STROMAL CELLS; SURVIVAL RATE;

EID: 77958616353     PISSN: 00039985     EISSN: 15432165     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Kaipainen A, Korhonen J, Mustonen T, et al. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci U S A. 1995;92(8):3566-3570.
2. Banerji S, Ni J, Wang SX, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol. 1999; 144(4):789-801.
3. Kato Y, Kaneko MK, Kuno A, et al. Inhibition of tumor cell-induced platelet aggregation using a novel anti-podoplanin antibody reacting with its plateletaggregation- stimulating domain. Biochem Biophys Res Commun. 2006;349(4): 1301-1307.
4. Gurleyik G, Gurleyik E, Aker F, et al. Lymphovascular invasion, as a prognostic marker in patients with invasive breast cancer. Acta Chir Belg. 2007; 107(3):284-287.
5. Horikawa YKT, Narita S, Inoue T, et al. Lymphatic invasion is a prognostic factor for bladder cancer treated with radical cystectomy. Int J Clin Oncol. 2007; 12(2):131-136.
6. General rules for clinical and pathological studies on cancer of the colon, rectum and anus. 7th ed. Japanese Research Society for Cancer of the Colon and Rectum. Tokyo, Japan: Kanehara Publisher; 2006.
7. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M. Upregulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol. 2005;166(3):913-921.
8. Kato Y, Kaneko M, Sata M, Fujita N, Tsuruo T, Osawa M. Enhanced expression of Aggrus (T1alpha/podoplanin), a platelet-aggregation-inducing factor in lung squamous cell carcinoma. Tumour Biol. 2005;26(4):195-200.
9. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, Christofori G. Tumor invasion in the absence of epithelial-mesenchymal transition: podoplaninmediated remodeling of the actin cytoskeleton. Cancer Cell. 2006;9(4):261-272.
10. Yuan P, Temam S, El-Naggar A, et al. Overexpression of podoplanin in oral cancer and its association with poor clinical outcome. Cancer. 2006;107(3): 563-569.
11. Kimura N, Kimura I. Podoplanin as a marker for mesothelioma. Pathol Int. 2005;55(2):83-86.
12. Ordonez NG. D2-40 and podoplanin are highly specific and sensitive immunohistochemical markers of epithelioid malignant mesothelioma. Hum Pathol. 2005;36(4):372-380.
13. Breiteneder-Geleff S, Soleiman A, Kowalski H, et al. Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am J Pathol. 1999; 154(2):385-394.
14. Roy S, Chu A, Trojanowski JQ, Zhang PJ. D2-40, a novel monoclonal antibody against the M2A antigen as a marker to distinguish hemangioblastomas from renal cell carcinomas. Acta Neuropathol (Berl). 2005;109(5):497-502.
15. Shibahara J, Kashima T, Kikuchi Y, Kunita A, Fukayama M. Podoplanin is expressed in subsets of tumors of the central nervous system. Virchows Arch. 2006;448(4):493-499.
16. Mishima K, Kato Y, Kaneko MK, et al. Podoplanin expression in primary central nervous system germ cell tumors: a useful histological marker for the diagnosis of germinoma. Acta Neuropathol (Berl). 2006;111(6):563-568.
17. Mishima K, Kato Y, Kaneko MK, Nishikawa R, Hirose T, Matsutani M. Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression. Acta Neuropathol (Berl). 2006; 111(5):483-488.
18. Aishima S, Nishihara Y, Iguchi T, et al. Lymphatic spread is related to VEGF-C expression and D2-40-positive myofibroblasts in intrahepatic cholangiocarcinoma. Mod Pathol. 2008;21(3):256-264.
19. Kawase A, Ishii G, Nagai K, et al. Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer. 2008;123(5):1053-1059.
20. Fukuoka J, Fujii T, Shih JH, et al. Chromatin remodeling factors and BRM/ BRG1 expression as prognostic indicators in non-small cell lung cancer. Clin Cancer Res. 2004;10(13):4314-4324.
21. Kononen J, Bubendorf L, Kallioniemi A, et al. Tissue microarrays for highthroughput molecular profiling of tumor specimens. Nat Med. 1998;4(7):844-847.
22. Kono T, Shimoda M, Takahashi M, et al. Immunohistochemical detection of the lymphatic marker podoplanin in diverse types of human cancer cells using a novel antibody. Int J Oncol. 2007;31(3):501-508.
23. Fukuoka J, Dracheva T, Shih JH, et al. Desmoglein 3 as a prognostic factor in lung cancer. Hum Pathol. 2007;38(2):276-283.
24. Camp RL, Charette LA, Rimm DL. Validation of tissue microarray technology in breast carcinoma. Lab Invest. 2000;80(12):1943-1949.
25. Yan G, Zhou XY, Cai SJ, Zhang GH, Peng JJ, Du X. Lymphangiogenic and angiogenic microvessel density in human primary sporadic colorectal carcinoma. World J Gastroenterol. 2008;14(1):101-107.
26. Ishikawa S, Takenaka K, Yanagihara K, et al. Matrix metalloproteinase-2 status in stromal fibroblasts, not in tumor cells, is a significant prognostic factor in non-small-cell lung cancer. Clin Cancer Res. 2004;10(19):6579-6585.
27. Yang G, Rosen DG, Zhang Z, et al. The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. Proc Natl Acad Sci U S A. 2006;103(44):16472-16477.
28. Renyi-Vamos F, Tovari J, Fillinger J, et al. Lymphangiogenesis correlates with lymph node metastasis, prognosis, and angiogenic phenotype in human non-small cell lung cancer. Clin Cancer Res. 2005;11(20):7344-7353.
29. Miyata Y, Kanda S, Ohba K, et al. Lymphangiogenesis and angiogenesis in bladder cancer: prognostic implications and regulation by vascular endothelial growth factors-A, -C, and -D. Clin Cancer Res. 2006;12(3, pt 1):800-806.
30. Kyzas PA, Geleff S, Batistatou A, Agnantis NJ, Stefanou D. Evidence for lymphangiogenesis and its prognostic implications in head and neck squamous cell carcinoma. J Pathol. 2005;206(2):170-177. (Pubitemid 40754020)
31. Royston D, Jackson DG. Mechanisms of lymphatic metastasis in human colorectal adenocarcinoma. J Pathol. 2009;217(5):608-619.
32. Infante JR, Matsubayashi H, Sato N, et al. Peritumoral fibroblast SPARC expression and patient outcome with resectable pancreatic adenocarcinoma. J Clin Oncol. 2007;25(3):319-325.
33. Koukourakis MI, Giatromanolaki A, Brekken RA, et al. Enhanced expression of SPARC/osteonectin in the tumor-associated stroma of non-small cell lung cancer is correlated with markers of hypoxia/acidity and with poor prognosis of patients. Cancer Res. 2003;63(17):5376-5380.
34. Cardillo MR, Ippoliti F. IL-6, IL-10 and HSP-90 expression in tissue microarrays from human prostate cancer assessed by computer-assisted image analysis. Anticancer Res. 2006;26(5A):3409-3416.
35. Ioachim E, Michael M, Stavropoulos NE, Kitsiou E, Salmas M, Malamou- Mitsi V. A clinicopathological study of the expression of extracellular matrix components in urothelial carcinoma. BJU Int. 2005;95(4):655-659.
36. Leivonen M, Lundin J, Nordling S, von Boguslawski K, Haglund C. Prognostic value of syndecan-1 expression in breast cancer. Oncology. 2004; 67(1):11-18.
37. Srivani R, Nagarajan B. A prognostic insight on in vivo expression of interleukin-6 in uterine cervical cancer. Int J Gynecol Cancer. 2003;13(3):331-339.
38. Surowiak P, Suchocki S, Gyorffy B, et al. Stromal myofibroblasts in breast cancer: relations between their occurrence, tumor grade and expression of some tumour markers. Folia Histochem Cytobiol. 2006;44(2):111-116.
39. Sutton CD, O'Byrne K, Goddard JC, et al. Expression of thrombospondin-1 in resected colorectal liver metastases predicts poor prognosis. Clin Cancer Res. 2005;11(18):6567-6573.
40. Yasuno M, Mori T, Koike M, et al. Importance of thymidine phosphorylase expression in tumor stroma as a prognostic factor in patients with advanced colorectal carcinoma. Oncol Rep. 2005;13(3):405-412.
41. Mylona E, Nomikos A, Magkou C, et al. The clinicopathological and prognostic significance of membrane type 1 matrix metalloproteinase (MT1- MMP) and MMP-9 according to their localization in invasive breast carcinoma. Histopathology. 2007;50(3):338-347.
42. Makretsov NA, Hayes M, Carter BA, Dabiri S, Gilks CB, Huntsman DG. Stromal CD10 expression in invasive breast carcinoma correlates with poor prognosis, estrogen receptor negativity, and high grade. Mod Pathol. 2007;20(1):84-89.
43. Kodama J, Hasengaowa, Kusumoto T, et al. Prognostic significance of stromal versican expression in human endometrial cancer. Ann Oncol. 2007; 18(2):269-274. (Pubitemid 46323092)
44. Cleven AH, van Engeland M, Wouters BG, de Bruine AP. Stromal expression of hypoxia regulated proteins is an adverse prognostic factor in colorectal carcinomas. Cell Oncol. 2007;29(3):229-240.
45. Orimo A, Gupta PB, Sgroi DC, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121(3):335-348.
46. Liang P, Hong JW, Ubukata H, et al. Myofibroblasts correlate with lymphatic microvessel density and lymph node metastasis in early-stage invasive colorectal carcinoma. Anticancer Res. 2005;25(4):2705-2712.
47. De Wever O, Mareel M. Role of tissue stroma in cancer cell invasion. J Pathol. 2003;200(4):429-447.
48. Direkze NC, Alison MR. Bone marrow and tumour stroma: an intimate relationship. Hematol Oncol. 2006;24(4):189-195.
49. Ishii G, Sangai T, Oda T, et al. Bone-marrow-derived myofibroblasts contribute to the cancer-induced stromal reaction. Biochem Biophys Res Commun. 2003;309(1):232-240.
50. Zuber M SG, Kocher T, Lüscher U, et al. Heterogeneity of melanoma antigen-1 (MAGE-1) gene and protein expression in malignant melanoma. Eur Surg Res. 1997;29(5):403-410.