Podocalyxin enhances breast tumor growth and metastasis and is a target for monoclonal antibody therapy

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Snyder, Kimberly A ^a   Hughes, Michael R ^a   Hedberg, Bradley ^a   Brandon, Jill ^a   Hernaez, Diana Canals ^a   Bergqvist, Peter ^a   Cruz, Frederic ^a   Po, Kelvin ^a   Graves, Marcia L ^a   Turvey, Michelle E ^b   Nielsen, Julie S ^a   Wilkins, John A ^c   McColl, Shaun R ^b   Babcook, John S ^a   Roskelley, Calvin D ^a   McNagny, Kelly M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; PODOCALYXIN; SHORT HAIRPIN RNA; ANTINEOPLASTIC AGENT; SIALOGLYCOPROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; BREAST CANCER CELL LINE; BREAST TUMOR; CANCER IMMUNOTHERAPY; CELL STRUCTURE; CONTROLLED STUDY; DISTANT METASTASIS; FEMALE; GENE; GENE DELETION; GENE OVEREXPRESSION; GENE SILENCING; GROWTH; HUMAN; HUMAN CELL; IMMUNOTHERAPY; IN VITRO STUDY; LIVER; LUNG; LUNG METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PODXL GENE; PRIMARY TUMOR; PROTEIN EXPRESSION; SYSTEMIC THERAPY; TUMOR ENGRAFTMENT; TUMOR GROWTH; TUMOR INVASION; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL TRANSFORMATION; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; EXPERIMENTAL MAMMARY NEOPLASM; GENETICS; METABOLISM; METASTASIS; MORTALITY; MULTICELLULAR SPHEROID; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL CULTURE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MICE; NEOPLASM METASTASIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIALOGLYCOPROTEINS; SPHEROIDS, CELLULAR; TUMOR BURDEN; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84928895865     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0562-7     Document Type: Article

References (37)

1. Weigelt B, Peterse JL, van 't Veer LJ. Breast cancer metastasis: markers and models. Nat Rev Cancer. 2005;5:591-602.
2. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13:4429-34.
3. Schopperle WM, DeWolf WC. The TRA-1-60 and TRA-1-81 human pluripotent stem cell markers are expressed on podocalyxin in embryonal carcinoma. Stem Cells. 2007;25:723-30.
4. Kelley TW, Huntsman D, McNagny KM, Roskelley CD, Hsi ED. Podocalyxin: a marker of blasts in acute leukemia. Am J Clin Pathol. 2005;124:134-42.
5. Graf T, McNagny K, Brady G, Frampton J. Chicken "erythroid" cells transformed by the Gag-Myb-Ets-encoding E26 leukemia virus are multipotent. Cell. 1992;70:201-13.
6. Schopperle WM, Kershaw DB, DeWolf WC. Human embryonal carcinoma tumor antigen, Gp200/GCTM-2, is podocalyxin. Biochem Biophys Res Commun. 2003;300:285-90.
7. Doyonnas R, Kershaw DB, Duhme C, Merkens H, Chelliah S, Graf T, et al. Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J Exp Med. 2001;194:13-27.
8. Nielsen JS, McNagny KM. The role of podocalyxin in health and disease. J Am Soc Nephrol. 2009;20:1669-76.
9. Strilic B, Kucera T, Eglinger J, Hughes MR, McNagny KM, Tsukita S, et al. The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell. 2009;17:505-15.
10. Somasiri A, Nielsen JS, Makretsov N, McCoy ML, Prentice L, Gilks CB, et al. Overexpression of the anti-adhesin podocalyxin is an independent predictor of breast cancer progression. Cancer Res. 2004;64:5068-73.
11. Binder ZA, Siu IM, Eberhart CG, ap Rhys C, Bai RY, Staedtke V, et al. Podocalyxin-like protein is expressed in glioblastoma multiforme stem-like cells and is associated with poor outcome. PLoS One. 2013;8:e75945.
12. Boman K, Larsson AH, Segersten U, Kuteeva E, Johannesson H, Nodin B, et al. Membranous expression of podocalyxin-like protein is an independent factor of poor prognosis in urothelial bladder cancer. Br J Cancer. 2013;108:2321-8.
13. Cipollone JA, Graves ML, Kobel M, Kalloger SE, Poon T, Gilks CB, et al. The anti-adhesive mucin podocalyxin may help initiate the transperitoneal metastasis of high grade serous ovarian carcinoma. Clin Exp Metastasis. 2012;29:239-52.
14. Dallas MR, Chen SH, Streppel MM, Sharma S, Maitra A, Konstantopoulos K. Sialofucosylated podocalyxin is a functional E- and L-selectin ligand expressed by metastatic pancreatic cancer cells. Am J Physiol Cell Physiol. 2012;303:C616-24.
15. Hsu YH, Lin WL, Hou YT, Pu YS, Shun CT, Chen CL, et al. Podocalyxin EBP50 ezrin molecular complex enhances the metastatic potential of renal cell carcinoma through recruiting Rac1 guanine nucleotide exchange factor ARHGEF7. Am J Pathol. 2010;176:3050-61.
16. Larsson A, Fridberg M, Gaber A, Nodin B, Leveen P, Jonsson G, et al. Validation of podocalyxin-like protein as a biomarker of poor prognosis in colorectal cancer. BMC Cancer. 2012;12:282.
17. Wu H, Yang L, Liao D, Chen Y, Wang W, Fang J. Podocalyxin regulates astrocytoma cell invasion and survival against temozolomide. Exp Ther Med. 2013;5:1025-9.
18. Yasuoka H, Tsujimoto M, Inagaki M, Kodama R, Tsuji H, Iwahashi Y, et al. Clinicopathological significance of podocalyxin and phosphorylated ezrin in uterine endometrioid adenocarcinoma. J Clin Pathol. 2012;65:399-402.
19. Nielsen JS, Graves ML, Chelliah S, Vogl AW, Roskelley CD, McNagny KM. The CD34-related molecule podocalyxin is a potent inducer of microvillus formation. PLoS One. 2007;2:e237.
20. Sizemore S, Cicek M, Sizemore N, Ng KP, Casey G. Podocalyxin increases the aggressive phenotype of breast and prostate cancer cells in vitro through its interaction with ezrin. Cancer Res. 2007;67:6183-91.
21. Meng X, Ezzati P, Wilkins JA. Requirement of podocalyxin in TGF-β induced epithelial mesenchymal transition. PLoS One. 2011;6:e18715.
22. McNagny KM, Hughes MR, Graves ML, DeBruin EJ, Snyder K, Cipollone J, et al. Podocalyxin in the diagnosis and treatment of cancer. In: Mohan R, editor. Advances in cancer management. Rijeka, Croatia: InTech; 2012. p. 155-94.
23. Lacroix M, Leclercq G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat. 2004;83:249-89.
24. Paxson JA, Gruntman A, Parkin CD, Mazan MR, Davis A, Ingenito EP, et al. Age-dependent decline in mouse lung regeneration with loss of lung fibroblast clonogenicity and increased myofibroblastic differentiation. PLoS One. 2011;6:e23232.
25. Babcook JS, Leslie KB, Olsen OA, Salmon RA, Schrader JW. A novel strategy for generating monoclonal antibodies from single, isolated lymphocytes producing antibodies of defined specificities. Proc Natl Acad Sci U S A. 1996;93:7843-8.
26. Ao A, Morrison BJ, Wang H, López JA, Reynolds BA, Lu J. Response of estrogen receptor-positive breast cancer tumorspheres to antiestrogen treatments. PLoS One. 2011;6:e18810.
27. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, Chiapero-Stanke L, et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res. 2008;10:R52.
28. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 2005;65:5506-11.
29. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17:1253-70.
30. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 2008;10:R25.
31. Larsson A, Johansson ME, Wangefjord S, Gaber A, Nodin B, Kucharzewska P, et al. Overexpression of podocalyxin-like protein is an independent factor of poor prognosis in colorectal cancer. Br J Cancer. 2011;105:666-72.
32. Larsson AH, Nodin B, Syk I, Palmquist I, Uhlén M, Eberhard J, et al. Podocalyxin-like protein expression in primary colorectal cancer and synchronous lymph node metastases. Diagn Pathol. 2013;8:109.
33. Debruin EJ, Hughes MR, Sina C, Liu A, Cait J, Jian Z, et al. Podocalyxin regulates murine lung vascular permeability by altering endothelial cell adhesion. PLoS One. 2014;9:e108881.
34. Blanchet MR, Bennett JL, Gold MJ, Levantini E, Tenen DG, Girard M, et al. CD34 is required for dendritic cell trafficking and pathology in murine hypersensitivity pneumonitis. Am J Respir Crit Care Med. 2011;184:687-98.
35. Doyonnas R, Nielsen JS, Chelliah S, Drew E, Hara T, Miyajima A, et al. Podocalyxin is a CD34-related marker of murine hematopoietic stem cells and embryonic erythroid cells. Blood. 2005;105:4170-8.
36. Nielsen JS, McNagny KM. Novel functions of the CD34 family. J Cell Sci. 2008;121:3683-92.
37. Lin CW, Sun MS, Liao MY, Chung CH, Chi YH, Chiou LT, et al. Podocalyxin-like 1 promotes invadopodia formation and metastasis through activation of Rac1/Cdc42/cortactin signaling in breast cancer cells. Carcinogenesis. 2014;35:2425-35.