Significance of podoplanin expression in cancer-associated fibroblasts: A comprehensive review
- Authors:
- Bartosz Pula
- Wojciech Witkiewicz
- Piotr Dziegiel
- Marzena Podhorska-Okolow
-
Affiliations: Regional Specialist Hospital, Research and Development Center, 51-124 Wroclaw, Poland, Department of Histology and Embryology, Medical University of Wroclaw, 50-368 Wroclaw, Poland - Published online on: April 8, 2013 https://doi.org/10.3892/ijo.2013.1887
- Pages: 1849-1857
This article is mentioned in:
Abstract
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Balkwill F and Mantovani A: Inflammation and cancer: back to Virchow? Lancet. 357:539–545. 2001. View Article : Google Scholar : PubMed/NCBI | |
Balkwill FR and Mantovani A: Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol. 22:33–40. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ruffell B, Affara NI and Coussens LM: Differential macrophage programming in the tumor microenvironment. Trends Immunol. 33:119–126. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kalluri R and Zeisberg M: Fibroblasts in cancer. Nat Rev Cancer. 6:392–401. 2006. View Article : Google Scholar | |
Parsonage G, Filer AD, Haworth O, et al: A stromal address code defined by fibroblasts. Trends Immunol. 26:150–156. 2005. View Article : Google Scholar : PubMed/NCBI | |
Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C and Brown RA: Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 3:349–363. 2002. View Article : Google Scholar : PubMed/NCBI | |
Allen M and Louise Jones J: Jekyll and Hyde: the role of the microenvironment on the progression of cancer. J Pathol. 223:162–176. 2011. View Article : Google Scholar : PubMed/NCBI | |
Simian M, Hirai Y, Navre M, Werb Z, Lochter A and Bissell MJ: The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development. 128:3117–3131. 2001.PubMed/NCBI | |
Bucala R: Review series - inflammation and fibrosis. Fibrocytes and fibrosis. QJM. 105:505–508. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hanahan D and Weinberg RA: Hallmarks of cancer: the next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI | |
Pietras K and Ostman A: Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res. 316:1324–1331. 2010. View Article : Google Scholar : PubMed/NCBI | |
Allinen M, Beroukhim R, Cai L, et al: Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 6:17–32. 2004. View Article : Google Scholar : PubMed/NCBI | |
Potenta S, Zeisberg E and Kalluri R: The role of endothelial-to-mesenchymal transition in cancer progression. Br J Cancer. 99:1375–1379. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zeisberg EM, Potenta S, Xie L, Zeisberg M and Kalluri R: Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 67:10123–10128. 2007.PubMed/NCBI | |
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. 121:335–348. 2005. View Article : Google Scholar : PubMed/NCBI | |
Boire A, Covic L, Agarwal A, Jacques S, Sherifi S and Kuliopulos A: PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell. 120:303–313. 2005. View Article : Google Scholar : PubMed/NCBI | |
Sternlicht MD, Lochter A, Sympson CJ, et al: The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell. 98:137–146. 1999. View Article : Google Scholar : PubMed/NCBI | |
Cheng N, Bhowmick NA, Chytil A, et al: Loss of TGF-beta type II receptor in fibroblasts promotes mammary carcinoma growth and invasion through upregulation of TGF-alpha-, MSP- and HGF-mediated signaling networks. Oncogene. 24:5053–5068. 2005. View Article : Google Scholar : PubMed/NCBI | |
Bhowmick NA, Chytil A, Plieth D, et al: TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science. 303:848–851. 2004. View Article : Google Scholar : PubMed/NCBI | |
Duncan MR, Frazier KS, Abramson S, et al: Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: down-regulation by cAMP. FASEB J. 13:1774–1786. 1999.PubMed/NCBI | |
Yang F, Tuxhorn JA, Ressler SJ, McAlhany SJ, Dang TD and Rowley DR: Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Cancer Res. 65:8887–8895. 2005. View Article : Google Scholar : PubMed/NCBI | |
Levental KR, Yu H, Kass L, et al: Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 139:891–906. 2009. View Article : Google Scholar : PubMed/NCBI | |
Erez N, Truitt M, Olson P, Arron ST and Hanahan D: Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell. 17:135–147. 2010. View Article : Google Scholar : PubMed/NCBI | |
Vermeulen L, De Sousa EMF, van der Heijden M, et al: Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol. 12:468–476. 2010. View Article : Google Scholar : PubMed/NCBI | |
de Sousa EM, Vermeulen L, Richel D and Medema JP: Targeting Wnt signaling in colon cancer stem cells. Clin Cancer Res. 17:647–653. 2011.PubMed/NCBI | |
Chang HY, Chi JT, Dudoit S, et al: Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA. 99:12877–12882. 2002. View Article : Google Scholar : PubMed/NCBI | |
Pula B, Jethon A, Piotrowska A, et al: Podoplanin expression by cancer-associated fibroblasts predicts poor outcome in invasive ductal breast carcinoma. Histopathology. 59:1249–1260. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kawase A, Ishii G, Nagai K, et al: Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer. 123:1053–1059. 2008. View Article : Google Scholar : PubMed/NCBI | |
Mork C, van Deurs B and Petersen OW: Regulation of vimentin expression in cultured human mammary epithelial cells. Differentiation. 43:146–156. 1990. View Article : Google Scholar : PubMed/NCBI | |
Strutz F, Okada H, Lo CW, et al: Identification and characterization of a fibroblast marker: FSP1. J Cell Biol. 130:393–405. 1995. View Article : Google Scholar : PubMed/NCBI | |
Rettig WJ, Garin-Chesa P, Healey JH, et al: Regulation and heteromeric structure of the fibroblast activation protein in normal and transformed cells of mesenchymal and neuroectodermal origin. Cancer Res. 53:3327–3335. 1993.PubMed/NCBI | |
Huber MA, Kraut N, Park JE, et al: Fibroblast activation protein: differential expression and serine protease activity in reactive stromal fibroblasts of melanocytic skin tumors. J Invest Dermatol. 120:182–188. 2003. View Article : Google Scholar | |
Lai D, Ma L and Wang F: Fibroblast activation protein regulates tumor-associated fibroblasts and epithelial ovarian cancer cells. Int J Oncol. 41:541–550. 2012.PubMed/NCBI | |
Sugimoto H, Mundel TM, Kieran MW and Kalluri R: Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther. 5:1640–1646. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kitano H, Kageyama S, Hewitt SM, et al: Podoplanin expression in cancerous stroma induces lymphangiogenesis and predicts lymphatic spread and patient survival. Arch Pathol Lab Med. 134:1520–1527. 2010.PubMed/NCBI | |
Schoppmann SF, Berghoff A, Dinhof C, et al: Podoplanin-expressing cancer-associated fibroblasts are associated with poor prognosis in invasive breast cancer. Breast Cancer Res Treat. Nov 19–2012.(Epub ahead of print). | |
Yamanashi T, Nakanishi Y, Fujii G, et al: Podoplanin expression identified in stromal fibroblasts as a favorable prognostic marker in patients with colorectal carcinoma. Oncology. 77:53–62. 2009. View Article : Google Scholar : PubMed/NCBI | |
Nose K, Saito H and Kuroki T: Isolation of a gene sequence induced later by tumor-promoting 12-O-tetradecanoylphorbol-13-acetate in mouse osteoblastic cells (MC3T3-E1) and expressed constitutively in ras-transformed cells. Cell Growth Differ. 1:511–518. 1990. | |
Wetterwald A, Hoffstetter W, Cecchini MG, et al: Characterization and cloning of the E11 antigen, a marker expressed by rat osteoblasts and osteocytes. Bone. 18:125–132. 1996. View Article : Google Scholar : PubMed/NCBI | |
Breiteneder-Geleff S, Matsui K, Soleiman A, et al: Podoplanin, novel 43-kd membrane protein of glomerular epithelial cells, is down-regulated in puromycin nephrosis. Am J Pathol. 151:1141–1152. 1997.PubMed/NCBI | |
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. 154:385–394. 1999. View Article : Google Scholar | |
Raica M, Cimpean AM and Ribatti D: The role of podoplanin in tumor progression and metastasis. Anticancer Res. 28:2997–3006. 2008.PubMed/NCBI | |
Marks A, Sutherland DR, Bailey D, et al: Characterization and distribution of an oncofetal antigen (M2A antigen) expressed on testicular germ cell tumours. Br J Cancer. 80:569–578. 1999. View Article : Google Scholar : PubMed/NCBI | |
Farr AG, Berry ML, Kim A, Nelson AJ, Welch MP and Aruffo A: Characterization and cloning of a novel glycoprotein expressed by stromal cells in T-dependent areas of peripheral lymphoid tissues. J Exp Med. 176:1477–1482. 1992. View Article : Google Scholar : PubMed/NCBI | |
Gandarillas A, Scholl FG, Benito N, Gamallo C and Quintanilla M: Induction of PA2.26, a cell-surface antigen expressed by active fibroblasts, in mouse epidermal keratinocytes during carcinogenesis. Mol Carcinog. 20:10–18. 1997. View Article : Google Scholar : PubMed/NCBI | |
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. 341:277–284. 1999. View Article : Google Scholar : PubMed/NCBI | |
Kato Y, Fujita N, Kunita A, et al: Molecular identification of Aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors. J Biol Chem. 278:51599–51605. 2003. View Article : Google Scholar : PubMed/NCBI | |
Schacht V, Ramirez MI, Hong YK, et al: T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 22:3546–3556. 2003. View Article : Google Scholar : PubMed/NCBI | |
Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong Y-K and Detmar M: Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol. 166:913–921. 2005. View Article : Google Scholar : PubMed/NCBI | |
Sonne SB, Herlihy AS, Hoei-Hansen CE, et al: Identity of M2A (D2-40) antigen and gp36 (Aggrus, T1A-2, podoplanin) in human developing testis, testicular carcinoma in situ and germ-cell tumours. Virchows Arch. 449:200–206. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kaneko MK, Kato Y, Kitano T and Osawa M: Conservation of a platelet activating domain of Aggrus/podoplanin as a platelet aggregation-inducing factor. Gene. 378:52–57. 2006. View Article : Google Scholar : PubMed/NCBI | |
Wicki A and Christofori G: The potential role of podoplanin in tumour invasion. Br J Cancer. 96:1–5. 2007. View Article : Google Scholar : PubMed/NCBI | |
Martin-Villar E, Yurrita MM, Fernandez-Munoz B, Quintanilla M and Renart J: Regulation of podoplanin/PA2.26 antigen expression in tumour cells. Involvement of calpain-mediated proteolysis. Int J Biochem Cell Biol. 41:1421–1429. 2009. View Article : Google Scholar : PubMed/NCBI | |
Martin-Villar E, Megias D, Castel S, Yurrita MM, Vilaro S and Quintanilla M: Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J Cell Sci. 119:4541–4553. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kriehuber E, Breiteneder-Geleff S, Groeger M, et al: Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med. 194:797–808. 2001. View Article : Google Scholar : PubMed/NCBI | |
Hwang YS, Xianglan Z, Park KK and Chung WY: Functional invadopodia formation through stabilization of the PDPN transcript by IMP-3 and cancer-stromal crosstalk for PDPN expression. Carcinogenesis. 33:2135–2146. 2012. View Article : Google Scholar : PubMed/NCBI | |
Honma M, Minami-Hori M, Takahashi H and Iizuka H: Podoplanin expression in wound and hyperproliferative psoriatic epidermis: regulation by TGF-beta and STAT-3 activating cytokines, IFN-gamma, IL-6, and IL-22. J Dermatol Sci. 65:134–140. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cortez MA, Nicoloso MS, Shimizu M, et al: miR-29b and miR-125a regulate podoplanin and suppress invasion in glioblastoma. Genes Chromosomes Cancer. 49:981–990. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D and Christofori G: Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell. 9:261–272. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kunita A, Kashima TG, Ohazama A, Grigoriadis AE and Fukayama M: Podoplanin is regulated by AP-1 and promotes platelet aggregation and cell migration in osteosarcoma. Am J Pathol. 179:1041–1049. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kreuger J, Nilsson I, Kerjaschki D, Petrova T, Alitalo K and Claesson-Welsh L: Early lymph vessel development from embryonic stem cells. Arterioscler Thromb Vasc Biol. 26:1073–1078. 2006. View Article : Google Scholar : PubMed/NCBI | |
Petrova TV, Makinen T, Makela TP, et al: Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 21:4593–4599. 2002. View Article : Google Scholar : PubMed/NCBI | |
Groger M, Loewe R, Holnthoner W, et al: IL-3 induces expression of lymphatic markers Prox-1 and podoplanin in human endothelial cells. J Immunol. 173:7161–7169. 2004. View Article : Google Scholar : PubMed/NCBI | |
Ramirez MI, Millien G, Hinds A, Cao Y, Seldin DC and Williams MC: T1alpha, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev Biol. 256:61–72. 2003. View Article : Google Scholar : PubMed/NCBI | |
Fu J, Gerhardt H, McDaniel JM, et al: Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J Clin Invest. 118:3725–3737. 2008. View Article : Google Scholar : PubMed/NCBI | |
Uhrin P, Zaujec J, Breuss JM, et al: Novel function for blood platelets and podoplanin in developmental separation of blood and lymphatic circulation. Blood. 115:3997–4005. 2010. View Article : Google Scholar : PubMed/NCBI | |
Suzuki-Inoue K, Kato Y, Inoue O, et al: Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem. 282:25993–26001. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kato Y, Kaneko MK, Kunita A, et al: Molecular analysis of the pathophysiological binding of the platelet aggregation-inducing factor podoplanin to the C-type lectin-like receptor CLEC-2. Cancer Sci. 99:54–61. 2008.PubMed/NCBI | |
Ogasawara S, Kaneko MK, Price JE and Kato Y: Characterization of anti-podoplanin monoclonal antibodies: critical epitopes for neutralizing the interaction between podoplanin and CLEC-2. Hybridoma. 27:259–267. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nieswandt B, Hafner M, Echtenacher B and Mannel DN: Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 59:1295–1300. 1999.PubMed/NCBI | |
Katagiri Y, Hayashi Y, Baba I, Suzuki H, Tanoue K and Yamazaki H: Characterization of platelet aggregation induced by the human melanoma cell line HMV-I: roles of heparin, plasma adhesive proteins, and tumor cell membrane proteins. Cancer Res. 51:1286–1293. 1991.PubMed/NCBI | |
Suzuki-Inoue K: Essential in vivo roles of the platelet activation receptor CLEC-2 in tumour metastasis, lymphangiogenesis and thrombus formation. J Biochem. 150:127–132. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kaneko MK, Kunita A, Abe S, et al: A chimeric anti-podoplanin antibody suppresses tumor metastasis via neutralization and antibody-dependent cellular cytotoxicity. Cancer Sci. 103:1913–1919. 2012. View Article : Google Scholar : PubMed/NCBI | |
Suzuki-Inoue K, Inoue O, Ding G, et al: Essential in vivo roles of the C-type lectin receptor CLEC-2: embryonic/neonatal lethality of CLEC-2-deficient mice by blood/lymphatic misconnections and impaired thrombus formation of CLEC-2-deficient platelets. J Biol Chem. 285:24494–24507. 2010. View Article : Google Scholar | |
May F, Hagedorn I, Pleines I, et al: CLEC-2 is an essential platelet-activating receptor in hemostasis and thrombosis. Blood. 114:3464–3472. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hughes CE, Navarro-Nunez L, Finney BA, Mourao-Sa D, Pollitt AY and Watson SP: CLEC-2 is not required for platelet aggregation at arteriolar shear. J Thromb Haemost. 8:2328–2332. 2010. View Article : Google Scholar : PubMed/NCBI | |
Cueni LN, Chen L, Zhang H, et al: Podoplanin-Fc reduces lymphatic vessel formation in vitro and in vivo and causes disseminated intravascular coagulation when transgenically expressed in the skin. Blood. 116:4376–4384. 2010. View Article : Google Scholar | |
Lowe KL, Navarro-Nunez L and Watson SP: Platelet CLEC-2 and podoplanin in cancer metastasis. Thromb Res. 129(Suppl 1): S30–S37. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest. 119:1420–1428. 2009. View Article : Google Scholar : PubMed/NCBI | |
Scholl FG, Gamallo C and Quintanilla M: Ectopic expression of PA2.26 antigen in epidermal keratinocytes leads to destabilization of adherens junctions and malignant progression. Lab Invest. 80:1749–1759. 2000. View Article : Google Scholar : PubMed/NCBI | |
Fernandez-Munoz B, Yurrita MM, Martin-Villar E, et al: The transmembrane domain of podoplanin is required for its association with lipid rafts and the induction of epithelial-mesenchymal transition. Int J Biochem Cell Biol. 43:886–896. 2011. View Article : Google Scholar : PubMed/NCBI | |
Martin-Villar E, Fernandez-Munoz B, Parsons M, et al: Podoplanin associates with CD44 to promote directional cell migration. Mol Biol Cell. 21:4387–4399. 2010. View Article : Google Scholar : PubMed/NCBI | |
Oliferenko S, Paiha K, Harder T, et al: Analysis of CD44-containing lipid rafts: recruitment of annexin II and stabilization by the actin cytoskeleton. J Cell Biol. 146:843–854. 1999. View Article : Google Scholar : PubMed/NCBI | |
Shen Y, Chen CS, Ichikawa H and Goldberg GS: SRC induces podoplanin expression to promote cell migration. J Biol Chem. 285:9649–9656. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hogan C: Impact of interactions between normal and transformed epithelial cells and the relevance to cancer. Cell Mol Life Sci. 69:203–213. 2012. View Article : Google Scholar : PubMed/NCBI | |
Acton SE, Astarita JL, Malhotra D, et al: Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity. 37:276–289. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cueni LN, Hegyi I, Shin JW, et al: Tumor lymphangiogenesis and metastasis to lymph nodes induced by cancer cell expression of podoplanin. Am J Pathol. 177:1004–1016. 2010. View Article : Google Scholar : PubMed/NCBI | |
Suzuki H, Onimaru M, Yonemitsu Y, Maehara Y, Nakamura S and Sueishi K: Podoplanin in cancer cells is experimentally able to attenuate prolymphangiogenic and lymphogenous metastatic potentials of lung squamoid cancer cells. Mol Cancer. 9:2872010. View Article : Google Scholar : PubMed/NCBI | |
Suzuki H, Onimaru M, Koga T, et al: High podoplanin expression in cancer cells predicts lower incidence of nodal metastasis in patients with lung squamous cell carcinoma. Pathol Res Pract. 207:111–115. 2011. View Article : Google Scholar : PubMed/NCBI | |
Dumoff KL, Chu C, Xu X, Pasha T, Zhang PJ and Acs G: Low D2-40 immunoreactivity correlates with lymphatic invasion and nodal metastasis in early-stage squamous cell carcinoma of the uterine cervix. Mod Pathol. 18:97–104. 2005. View Article : Google Scholar : PubMed/NCBI | |
Dumoff KL, Chu CS, Harris EE, et al: 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. 19:708–716. 2006. View Article : Google Scholar | |
Ito T, Ishii G, Nagai K, et al: Low podoplanin expression of tumor cells predicts poor prognosis in pathological stage IB squamous cell carcinoma of the lung, tissue microarray analysis of 136 patients using 24 antibodies. Lung Cancer. 63:418–424. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shimada Y, Ishii G, Nagai K, et al: Expression of podoplanin, CD44, and p63 in squamous cell carcinoma of the lung. Cancer Sci. 100:2054–2059. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yuan P, Temam S, El-Naggar A, et al: Overexpression of podoplanin in oral cancer and its association with poor clinical outcome. Cancer. 107:563–569. 2006. View Article : Google Scholar : PubMed/NCBI | |
Saigusa S, Mohri Y, Ohi M, et al: Podoplanin and SOX2 expression in esophageal squamous cell carcinoma after neoadjuvant chemo-radiotherapy. Oncol Rep. 26:1069–1074. 2011.PubMed/NCBI | |
Kreppel M, Drebber U, Wedemeyer I, et al: Podoplanin expression predicts prognosis in patients with oral squamous cell carcinoma treated with neoadjuvant radiochemotherapy. Oral Oncol. 47:873–878. 2011. View Article : Google Scholar : PubMed/NCBI | |
Tateyama H, Sugiura H, Yamatani C and Yano M: Expression of podoplanin in thymoma: its correlation with tumor invasion, nodal metastasis, and poor clinical outcome. Hum Pathol. 42:533–540. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kreppel M, Scheer M, Drebber U, Ritter L and Zoller JE: Impact of podoplanin expression in oral squamous cell carcinoma: clinical and histopathologic correlations. Virchows Arch. 456:473–482. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chuang WY, Yeh CJ, Wu YC, et al: Tumor cell expression of podoplanin correlates with nodal metastasis in esophageal squamous cell carcinoma. Histol Histopathol. 24:1021–1027. 2009.PubMed/NCBI | |
Chao YK, Chuang WY, Yeh CJ, et al: Prognostic significance of high podoplanin expression after chemoradiotherapy in esophageal squamous cell carcinoma patients. J Surg Oncol. 105:183–188. 2012. View Article : Google Scholar : PubMed/NCBI | |
Rahadiani N, Ikeda J, Makino T, et al: Tumorigenic role of podoplanin in esophageal squamous-cell carcinoma. Ann Surg Oncol. 17:1311–1323. 2010. View Article : Google Scholar : PubMed/NCBI | |
Atsumi N, Ishii G, Kojima M, Sanada M, Fujii S and Ochiai A: Podoplanin, a novel marker of tumor-initiating cells in human squamous cell carcinoma A431. Biochem Biophys Res Commun. 373:36–41. 2008. View Article : Google Scholar : PubMed/NCBI | |
Toll A, Gimeno-Beltran J, Ferrandiz-Pulido C, et al: D2-40 immunohistochemical overexpression in cutaneous squamous cell carcinomas: a marker of metastatic risk. J Am Acad Dermatol. 67:1310–1318. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kalof AN and Cooper K: D2-40 immunohistochemistry - so far! Adv Anat Pathol. 16:62–64. 2009. | |
Hoshino A, Ishii G, Ito T, et al: Podoplanin-positive fibroblasts enhance lung adenocarcinoma tumor formation: podoplanin in fibroblast functions for tumor progression. Cancer Res. 71:4769–4779. 2011. View Article : Google Scholar | |
Ito M, Ishii G, Nagai K, Maeda R, Nakano Y and Ochiai A: Prognostic impact of cancer-associated stromal cells in stage I lung adenocarcinoma patients. Chest. 142:151–158. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kadota K, Huang CL, Liu D, et al: The clinical significance of the tumor cell D2-40 immunoreactivity in non-small cell lung cancer. Lung Cancer. 70:88–93. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ito S, Ishii G, Hoshino A, et al: Tumor promoting effect of podoplanin-positive fibroblasts is mediated by enhanced RhoA activity. Biochem Biophys Res Commun. 422:194–199. 2012. View Article : Google Scholar : PubMed/NCBI | |
Neri S, Ishii G, Taira T, et al: Recruitment of podoplanin positive cancer-associated fibroblasts in metastatic lymph nodes predicts poor prognosis in pathological N2 stage III lung adenocarcinoma. Ann Surg Oncol. 19:3953–3962. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ono S, Ishii G, Nagai K, et al: Podoplanin-positive cancer associated fibroblast could have prognostic value independent of cancer cell phenotype in stage I lung squamous cell carcinoma: utility of combining analysis of both cancer cell phenotype and cancer associated fibroblast phenotype. Chest. Oct 15–2012.(Epub ahead of print). View Article : Google Scholar | |
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. 21:256–264. 2008. View Article : Google Scholar : PubMed/NCBI | |
Carvalho FM, Zaganelli FL, Almeida BG, Goes JC, Baracat EC and Carvalho JP: Prognostic value of podoplanin expression in intratumoral stroma and neoplastic cells of uterine cervical carcinomas. Clinics. 65:1279–1283. 2010. View Article : Google Scholar : PubMed/NCBI | |
Schoppmann SF, Jesch B, Riegler MF, et al: Podoplanin expressing cancer associated fibroblasts are associated with unfavourable prognosis in adenocarcinoma of the esophagus. Clin Exp Metastasis. 30:441–446. 2013. View Article : Google Scholar : PubMed/NCBI |