Podoplanin expression identified in stromal fibroblasts as a favorable prognostic marker in patients with colorectal carcinoma

Oncology

Volumn 77, Issue 1, 2009, Pages 53-62

  Yamanashi, Takahiro ^a,c   Nakanishi, Yukihiro ^a   Fujii, Gen ^a   Akishima Fukasawa, Yuri ^a   Moriya, Yoshihiro ^b   Kanai, Yae ^a   Watanabe, Masahiko ^c   Hirohashi, Setsuo ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b NATIONAL CANCER CENTER HOSPITAL   (Japan)

^c KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Clinicopathologic study; Colorectal cancer; Immunohistochemistry; Podoplanin; Prognosis

Indexed keywords

PODOPLANIN; SMALL INTERFERING RNA; TUMOR MARKER; COLLAGEN; LAMININ; MATRIGEL; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN; PROTEOGLYCAN;

ADULT; ADVANCED CANCER; AGED; ARTICLE; CANCER INVASION; CELL STRAIN; CELL STRAIN HCT116; CELL STRAIN HCT15; COCULTURE; COLORECTAL CARCINOMA; DISEASE FREE SURVIVAL; DNA MICROARRAY; FEMALE; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; JAPAN; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGNOSIS; TUMOR LOCALIZATION; ADENOCARCINOMA; CANCER STAGING; CELL CULTURE; COLORECTAL TUMOR; CULTURE MEDIUM; DRUG ANTAGONISM; DRUG COMBINATION; ENZYME IMMUNOASSAY; GENETICS; METABOLISM; METASTASIS; MIDDLE AGED; PATHOLOGY; STROMA CELL; SURVIVAL RATE; WESTERN BLOTTING;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; CELLS, CULTURED; COLLAGEN; COLORECTAL NEOPLASMS; CULTURE MEDIA, CONDITIONED; DRUG COMBINATIONS; FEMALE; FIBROBLASTS; HUMANS; IMMUNOENZYME TECHNIQUES; LAMININ; LYMPHATIC METASTASIS; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; PROTEOGLYCANS; RNA, SMALL INTERFERING; STROMAL CELLS; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 67649221971     PISSN: 00302414     EISSN: None     Source Type: Journal    
DOI: 10.1159/000226112     Document Type: Article

References (50)

1. Bhowmick NA, Neilson EG, Moses HL: Stromal fibroblasts in cancer initiation and progression. Nature 2004;432:332-337.
2. De Wever O, Mareel M: Role of tissue stroma in cancer cell invasion. J Pathol 2003;200:429-447.
3. Kalluri R, Zeisberg M: Fibroblasts in cancer. Nat Rev Cancer 2006;6:392-401.
4. Micke P, Ostman A: Exploring the tumour environment: cancer-associated fibroblasts as targets in cancer therapy. Expert Opin Ther Targets 2005;9:1217-1233.
5. Bhowmick NA, Chytil A, Plieth D, et al: TGF-β signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004;303:848-851.
6. 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;121:335-348.
7. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR: Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 1999;59:5002-5011.
8. Dimanche-Boitrel MT, Vakaet L Jr, Pujuguet P, et al: In vivo and in vitro invasiveness of a rat colon-cancer cell line maintaining E-cadherin expression: an enhancing role of tumor-associated myofibroblasts. Int J Cancer 1994;56:512-521.
9. Sternlicht MD, Lochter A, Sympson CJ, et al: The stromal proteinase MMP3/stromelysin1 promotes mammary carcinogenesis. Cell 1999;98:137-146.
10. Lochter A, Galosy S, Muschler J, Freedman N, Werb Z, Bissell MJ: Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable ep-ithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J Cell Biol 1997;139:1861-1872.
11. Cornil I, Theodorescu D, Man S, Herlyn M, Jambrosic J, Kerbel RS: Fibroblast cell interactions with human melanoma cells affect tumor cell growth as a function of tumor progression. Proc Natl Acad Sci USA 1991;88:6028-6032.
12. 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;111:483-488.
13. Yuan P, Temam S, El-Naggar A, et al: Over-expression of podoplanin in oral cancer and its association with poor clinical outcome. Cancer 2006;107:563-569.
14. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M: Up-regulation of the lymphatic marker podoplanin, a mucintype transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol 2005;166:913-921.
15. Zimmer G, Oeffner F, Von Messling V, et al: Cloning and characterization of gp36, a human mucin-type glycoprotein preferentially expressed in vascular endothelium. Biochem J 1999;341:277-284.
16. Brockhausen I, Schutzbach J, Kuhns W: Glycoproteins and their relationship to human disease. Acta Anat (Basel) 1998;161:36-78.
17. Martin-Villar E, Scholl FG, Gamallo C, et al: Characterization of human PA2.26 antigen (T1α-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int J Cancer 2005;113:899-910.
18. Ordonez NG: Podoplanin: a novel diagnostic immunohistochemical marker. Adv Anat Pathol 2006;13:83-88.
19. 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;154:385-394.
20. Schacht V, Ramirez MI, Hong YK, et al: T1α/ podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. Embo J 2003;22:3546-3556.
21. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, Christofori G: Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 2006;9:261-272.
22. Sugimoto Y, Watanabe M, Oh-hara T, Sato S, Isoe T, Tsuruo T: Suppression of experimental lung colonization of a metastatic variant of murine colon adenocarcinoma 26 by a monoclonal antibody 8F11 inhibiting tumor cell-induced platelet aggregation. Cancer Res 1991;51:921-925.
23. Watanabe M, Okochi E, Sugimoto Y, Tsuruo T: Identification of a platelet-aggregating factor of murine colon adenocarcinoma as determined by monoclonal antibodies. Cancer Res 1988;48:6411-6416.
24. Kato Y, Kaneko M, Sata M, Fujita N, Tsuruo T, Osawa M: Enhanced expression of Aggrus (T1α/podoplanin), a platelet-aggregation-inducing factor in lung squamous cell carcinoma. Tumour Biol 2005;26:195-200.
25. Kimura N, Kimura I: Podoplanin as a marker for mesothelioma. Pathol Int 2005;55:83-86.
26. Ordonez NG: D2-40 and podoplanin are highly specific and sensitive immunohistochemical markers of epithelioid malignant mesothelioma. Hum Pathol 2005;36:372-380.
27. 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;109:497-502.
28. Kato Y, Sasagawa I, Kaneko M, Osawa M, Fujita N, Tsuruo T: Aggrus: a diagnostic marker that distinguishes seminoma from embryonal carcinoma in testicular germ cell tumors. Oncogene 2004;23:8552-8556.
29. 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;448:493-499.
30. 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;111:563-568.
31. Gandarillas A, Scholl FG, Benito N, Gamallo C, Quintanilla M: Induction of PA2.26, a cell-surface antigen expressed by active fibroblasts, in mouse epidermal keratinocytes during carcinogenesis. Mol Carcinog 1997;20:10-18.
32. Sobin LH, Fleming ID: TNM Classification of Malignant Tumors, ed 5 (1997). Union Internationale contre le Cancer and the American Joint Committee on Cancer. Cancer 1997;80:1803-1804.
33. World Health Organization: Classification of Tumours. Lyon, IARC Press, 2000.
34. DeCosse JJ, Gossens C, Kuzma JF, Unsworth BR: Embryonic inductive tissues that cause histologic differentiation of murine mammary carcinoma in vitro. J Natl Cancer Inst 1975;54:913-922.
35. DeCosse JJ, Gossens CL, Kuzma JF, Un-sworth BR: Breast cancer: induction of differentiation by embryonic tissue. Science 1973;181:1057-1058.
36. Cooper M, Pinkus H: Intrauterine transplantation of rat basal cell carcinoma as a model for reconversion of malignant to benign growth. Cancer Res 1977;37:2544-2552.
37. Maehara N, Matsumoto K, Kuba K, Mizumoto K, Tanaka M, Nakamura T: NK4, a four-kringle antagonist of HGF, inhibits spreading and invasion of human pancreatic cancer cells. Br J Cancer 2001;84:864-873.
38. Gendler SJ, Spicer AP: Epithelial mucin genes. Annu Rev Physiol 1995;57:607-634.
39. Hilkens J, Ligtenberg MJ, Vos HL, Litvinov SV: Cell membrane-associated mucins and their adhesion-modulating property. Trends Biochem Sci 1992;17:359-363.
40. Vark i A: Selecti n l iga nds. Proc Natl Acad Sci USA 1994;91:7390 -7397.
41. Yuan P, Temam S, El-Naggar A, Zhou X, Liu DD, Lee JJ, Mao L: Overexpression of podoplanin in oral cancer and its association with poor clinical outcome. Cancer 2006;10 7:563-569.
42. Dumoff KL, Chu CS, Harris EE, Holtz D, Xu X, Zhang PJ, ACS G: Low podoplanin expression in pretreatment biopsy material predicts poor prognosis in advanced-stage squamous cell carcinoma of the uterine cervix treated by primary radiation. Mod Pathol 2006;19:708-716.
43. Ordonez NG: D2-40 and podoplanin are highly specific and sensitive immunohistochemical markers of epithelioid malignant mesothelioma. Hum Pathol 2005;36:372-380.
44. Chu AY, Litzky LA, Pasha TL, Acs G, Zhang PJ: Utility of D2-40, a novel mesothelial marker, in the diagnosis of malignant mesothelioma. Mod Pathol 2005;18:105-110.
45. Kawase A, Ishii G, Nagai K, Ito T, Nagano T, Murata Y, Hishida T, Nishimura M, Yoshida J, Suzuki K, Ochiai A: Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer 2008;123:1053-1059.
46. Okuyama T, Oya M, Ishikawa H: Budding as a risk factor for lymph node metastasis in pT1 or pT2 well-differentiated colorectal adenocarcinoma. Dis Colon Rectum 2002;45: 628-634.
47. Ueno H, Price AB, Wilkinson KH, Jass JR, Mochizuki H, Talbot IC: A new prognostic staging system for rectal cancer. Ann Surg 2004;240:832-839.
48. Barsky SH, Gopalakrishna R: Increased invasion and spontaneous metastasis of BL6 melanoma with inhibition of the desmoplastic response in C57 BL/6 mice. Cancer Res 1987;47:1663-1667.
49. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK: Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000;60:2497-2503.
50. Brown EB, Boucher Y, Nasser S, Jain RK: Measurement of macromolecular diffusion coefficients in human tumors. Microvasc Res 20 04;67:231-236.