CD147-Dependent heterogeneity in malignant and chemoresistant properties of cancer cells

American Journal of Pathology

Volumn 182, Issue 2, 2013, Pages 577-585

  Dai, Lu ^a,c   Guinea, Maria C ^a   Slomiany, Mark G ^a,d   Bratoeva, Momka ^a   Grass, G Daniel ^a   Tolliver, Lauren B ^a   Maria, Bernard L ^d   Toole, Bryan P ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CD147 ANTIGEN; HERMES ANTIGEN; MONOCARBOXYLATE TRANSPORTER 4; MULTIDRUG RESISTANCE PROTEIN 1;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENICITY; CELL HETEROGENEITY; CELL MEMBRANE; CELL SHAPE; CELL SUBPOPULATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD147; ANTIGENS, CD44; CELL ADHESION; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DRUG RESISTANCE, NEOPLASM; FEMALE; FLOW CYTOMETRY; GENETIC HETEROGENEITY; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; NEOPLASM INVASIVENESS; NEOPLASMS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SPHEROIDS, CELLULAR;

EID: 84872714824     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.10.011     Document Type: Article

References (56)

1. J.M. Rosen, and C.T. Jordan The increasing complexity of the cancer stem cell paradigm Science 324 2009 1670 1673
2. S. Liu, and M.S. Wicha Targeting breast cancer stem cells J Clin Oncol 28 2010 4006 4012
3. C.L. Chaffer, and R.A. Weinberg A perspective on cancer cell metastasis Science 331 2011 1559 1564
4. C.D. May, N. Sphyris, K.W. Evans, S.J. Werden, W. Guo, and S.A. Mani Epithelial-mesenchymal transition and cancer stem cells: a dangerously dynamic duo in breast cancer progression Breast Cancer Res 13 2011 202
5. H. Clevers The cancer stem cell: premises, promises and challenges Nat Med 17 2011 313 319
6. C.M. Fillmore, and C. Kuperwasser Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy Breast Cancer Res 10 2008 R25
7. E. Charafe-Jauffret, C. Ginestier, F. Iovino, J. Wicinski, N. Cervera, P. Finetti, M.H. Hur, M.E. Diebel, F. Monville, J. Dutcher, M. Brown, P. Viens, L. Xerri, F. Bertucci, G. Stassi, G. Dontu, D. Birnbaum, and M.S. Wicha Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature Cancer Res 69 2009 1302 1313
8. T. Muramatsu, and T. Miyauchi Basigin (CD147): a multifunctional transmembrane protein involved in reproduction, neural function, inflammation and tumor invasion Histol Histopathol 18 2003 981 987
9. L. Yan, S. Zucker, and B.P. Toole Roles of the multifunctional glycoprotein, emmprin (basigin; CD147), in tumour progression Thromb Haemost 93 2005 199 204
10. E.E. Gabison, T. Hoang-Xuan, A. Mauviel, and S. Menashi EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair Biochimie 87 2005 361 368
11. K. Nabeshima, H. Iwasaki, K. Koga, H. Hojo, J. Suzumiya, and M. Kikuchi Emmprin (basigin/CD147): matrix metalloproteinase modulator and multifunctional cell recognition molecule that plays a critical role in cancer progression Pathol Int 56 2006 359 367
12. S.M. Ellis, K. Nabeshima, and C. Biswas Monoclonal antibody preparation and purification of a tumor cell collagenase-stimulatory factor Cancer Res 49 1989 3385 3391
13. H. Kataoka, R. DeCastro, S. Zucker, and C. Biswas Tumor cell-derived collagenase-stimulatory factor increases expression of interstitial collagenase, stromelysin, and 72-kDa gelatinase Cancer Res 53 1993 3154 3158
14. C. Biswas, Y. Zhang, R. DeCastro, H. Guo, T. Nakamura, H. Kataoka, and K. Nabeshima The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily Cancer Res 55 1995 434 439
15. S. Zucker, M. Hymowitz, E.E. Rollo, R. Mann, C.E. Conner, J. Cao, H.D. Foda, D.C. Tompkins, and B.P. Toole Tumorigenic potential of extracellular matrix metalloproteinase inducer (EMMPRIN) Am J Pathol 158 2001 1921 1928
16. J. Sun, and M.E. Hemler Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions Cancer Res 61 2001 2276 2281
17. S. Caudroy, M. Polette, B. Nawrocki-Raby, J. Cao, B.P. Toole, S. Zucker, and P. Birembaut Emmprin-mediated MMP regulation in tumor and endothelial cells Clin Exp Metastasis 19 2002 697 702
18. Y. Tang, M.T. Nakada, P. Kesavan, F. McCabe, H. Millar, P. Rafferty, P. Bugelski, and L. Yan Extracellular matrix metalloproteinase inducer stimulates tumor angiogenesis by elevating vascular endothelial cell growth factor and matrix metalloproteinases Cancer Res 65 2005 3193 3199
19. C. Manoharan, M.C. Wilson, R.B. Sessions, and A.P. Halestrap The role of charged residues in the transmembrane helices of monocarboxylate transporter 1 and its ancillary protein basigin in determining plasma membrane expression and catalytic activity Mol Membr Biol 23 2006 486 498
20. S.M. Gallagher, J.J. Castorino, D. Wang, and N.J. Philp Monocarboxylate transporter 4 regulates maturation and trafficking of CD147 to the plasma membrane in the metastatic breast cancer cell line MDA-MB-231 Cancer Res 67 2007 4182 4189
21. A.A. Deora, N. Philp, J. Hu, D. Bok, and E. Rodriguez-Boulan Mechanisms regulating tissue-specific polarity of monocarboxylate transporters and their chaperone CD147 in kidney and retinal epithelia Proc Natl Acad Sci USA 102 2005 16245 16250
22. D. Xu, and M.E. Hemler Metabolic activation-related CD147-CD98 complex Mol Cell Proteomics 4 2005 1061 1071
23. W.J. Wang, Q.Q. Li, J.D. Xu, X.X. Cao, H.X. Li, F. Tang, Q. Chen, J.M. Yang, Z.D. Xu, and X.P. Liu Interaction between CD147 and P-glycoprotein and their regulation by ubiquitination in breast cancer cells Chemotherapy 54 2008 291 301
24. Z. Qin, L. Dai, M. Bratoeva, M.G. Slomiany, B.P. Toole, and C. Parsons Cooperative roles for emmprin and LYVE-1 in the regulation of chemoresistance for primary effusion lymphoma Leukemia 25 2011 1598 1609
25. G.D. Grass, M. Bratoeva, and B.P. Toole Regulation of invadopodia formation and activity by CD147 J Cell Sci 125 2012 777 788
26. M.G. Slomiany, G.D. Grass, A.D. Robertson, X.Y. Yang, B.L. Maria, B. Beeson, and B.P. Toole Hyaluronan, CD44 and emmprin regulate lactate efflux and membrane localization of monocarboxylate transporters in human breast carcinoma cells Cancer Res 69 2009 1293 1301
27. S. Misra, S. Ghatak, A. Zoltan-Jones, and B.P. Toole Regulation of multi-drug resistance in cancer cells by hyaluronan J Biol Chem 278 2003 25285 25288
28. Q.Q. Li, W.J. Wang, J.D. Xu, X.X. Cao, Q. Chen, J.M. Yang, and Z.D. Xu Involvement of CD147 in regulation of multidrug resistance to P-gp substrate drugs and in vitro invasion in breast cancer cells Cancer Sci 98 2007 1064 1069
29. M. Baba, M. Inoue, K. Itoh, and Y. Nishizawa Blocking CD147 induces cell death in cancer cells through impairment of glycolytic energy metabolism Biochem Biophys Res Commun 374 2008 111 116
30. Y.H. Kuang, X. Chen, J. Su, L.S. Wu, L.Q. Liao, D. Li, Z.S. Chen, and T. Kanekura RNA interference targeting the CD147 induces apoptosis of multi-drug resistant cancer cells related to XIAP depletion Cancer Lett 276 2009 189 195
31. J. Hao, H. Chen, M.C. Madigan, P.J. Cozzi, J. Beretov, W. Xiao, W.J. Delprado, P.J. Russell, and Y. Li Co-expression of CD147 (EMMPRIN), CD44v3-10, MDR1 and monocarboxylate transporters is associated with prostate cancer drug resistance and progression Br J Cancer 103 2010 1008 1018
32. E.A. Marieb, A. Zoltan-Jones, R. Li, S. Misra, S. Ghatak, J. Cao, S. Zucker, and B.P. Toole Emmprin promotes anchorage-independent growth in human mammary carcinoma cells by stimulating hyaluronan production Cancer Res 64 2004 1229 1232
33. X. Chen, J. Lin, T. Kanekura, J. Su, W. Lin, H. Xie, Y. Wu, J. Li, M. Chen, and J. Chang A small interfering CD147-targeting RNA inhibited the proliferation, invasiveness, and metastatic activity of malignant melanoma Cancer Res 66 2006 11323 11330
34. J. Xu, H.Y. Xu, Q. Zhang, F. Song, J.L. Jiang, X.M. Yang, L. Mi, N. Wen, R. Tian, L. Wang, H. Yao, Q. Feng, Y. Zhang, J.L. Xing, P. Zhu, and Z.N. Chen HAb18G/CD147 functions in invasion and metastasis of hepatocellular carcinoma Mol Cancer Res 5 2007 605 614
35. J. Su, X. Chen, and T. Kanekura A CD147-targeting siRNA inhibits the proliferation, invasiveness, and VEGF production of human malignant melanoma cells by down-regulating glycolysis Cancer Lett 273 2009 140 147
36. K. Nabeshima, H. Iwasaki, J. Nishio, K. Koga, M. Shishime, and M. Kikuchi Expression of emmprin and matrix metalloproteinases (MMPs) in peripheral nerve sheath tumors: emmprin and membrane-type (MT)1-MMP expressions are associated with malignant potential Anticancer Res 26 2006 1359 1367
37. B. Davidson, I. Goldberg, A. Berner, G.B. Kristensen, and R. Reich EMMPRIN (extracellular matrix metalloproteinase inducer) is a novel marker of poor outcome in serous ovarian carcinoma Clin Exp Metastasis 20 2003 161 169
38. J.A. Ward, L. Huang, H. Guo, S. Ghatak, and B.P. Toole Perturbation of hyaluronan interactions inhibits malignant properties of glioma cells Am J Pathol 162 2003 1403 1409
39. R. Li, L. Huang, H. Guo, and B.P. Toole Basigin (murine EMMPRIN) stimulates matrix metalloproteinase production by fibroblasts J Cell Physiol 186 2001 371 379
40. L.W. Fu, Y.M. Zhang, Y.J. Liang, X.P. Yang, and Q.C. Pan The multidrug resistance of tumour cells was reversed by tetrandrine in vitro and in xenografts derived from human breast adenocarcinoma MCF-7/adr cells Eur J Cancer 38 2002 418 426
41. V.H. Freedman, and S.I. Shin Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium Cell 3 1974 355 359
42. X. Li, M.T. Lewis, J. Huang, C. Gutierrez, C.K. Osborne, M.F. Wu, S.G. Hilsenbeck, A. Pavlick, X. Zhang, G.C. Chamness, H. Wong, J. Rosen, and J.C. Chang Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy J Natl Cancer Inst 100 2008 672 679
43. S. Zhang, C. Balch, M.W. Chan, H.C. Lai, D. Matei, J.M. Schilder, P.S. Yan, T.H. Huang, and K.P. Nephew Identification and characterization of ovarian cancer-initiating cells from primary human tumors Cancer Res 68 2008 4311 4320
44. L.Y.W. Bourguignon Hyaluronan-mediated CD44 interaction with receptor and non-receptor kinases promotes oncogenic signaling, cytoskeleton activation and tumor progression. Hyaluronan in Cancer Biology R. Stern, 2009 Academic Press San Diego 89 107
45. B.P. Toole Hyaluronan-CD44 interactions in cancer: paradoxes and possibilities Clin Cancer Res 15 2009 7462 7468
46. M.G. Slomiany, L. Dai, L.B. Tolliver, G.D. Grass, Y. Zeng, and B.P. Toole Inhibition of functional hyaluronan-CD44 interactions in CD133-positive primary human ovarian carcinoma cells by small hyaluronan oligosaccharides Clin Cancer Res 15 2009 7593 7601
47. J.M. Yang, P. O'Neill, W. Jin, R. Foty, D.J. Medina, Z. Xu, M. Lomas, G.M. Arndt, Y. Tang, M. Nakada, L. Yan, and W.N. Hait Extracellular matrix metalloproteinase inducer (CD147) confers resistance of breast cancer cells to Anoikis through inhibition of Bim J Biol Chem 281 2006 9719 9727
48. K. Muraoka, K. Nabeshima, T. Murayama, C. Biswas, and M. Koono Enhanced expression of a tumor-cell-derived collagenase-stimulatory factor in urothelial carcinoma: its usefulness as a tumor marker for bladder cancers Int J Cancer 55 1993 19 26
49. M. Polette, C. Gilles, V. Marchand, M. Lorenzato, B. Toole, J.M. Tournier, S. Zucker, and P. Birembaut Tumor collagenase stimulatory factor (TCSF) expression and localization in human lung and breast cancers J Histochem Cytochem 45 1997 703 709
50. T. Sameshima, K. Nabeshima, B.P. Toole, K. Yokogami, Y. Okada, T. Goya, M. Koono, and S. Wakisaka Expression of emmprin (CD147), a cell surface inducer of matrix metalloproteinases, in normal human brain and gliomas Int J Cancer 88 2000 21 27
51. C.A. Klein, S. Seidl, K. Petat-Dutter, S. Offner, J.B. Geigl, O. Schmidt-Kittler, N. Wendler, B. Passlick, R.M. Huber, G. Schlimok, P.A. Baeuerle, and G. Riethmüller Combined transcriptome and genome analysis of single micrometastatic cells Nature Biotechnol 20 2002 387 392
52. T. Kanekura, X. Chen, and T. Kanzaki Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metalloproteinases by fibroblasts Int J Cancer 99 2002 520 528
53. B. Davidson, V. Givant-Horwitz, P. Lazarovici, B. Risberg, J.M. Nesland, C.G. Trope, E. Schaefer, and R. Reich Matrix metalloproteinases (MMP), EMMPRIN (extracellular matrix metalloproteinase inducer) and mitogen-activated protein kinases (MAPK): co-expression in metastatic serous ovarian carcinoma Clin Exp Metastasis 20 2003 621 631
54. S. Ghatak, S. Misra, and B.P. Toole Hyaluronan regulates constitutive ErbB2 phosphorylation and signal complex formation in carcinoma cells J Biol Chem 280 2005 8875 8883
55. M. Zöller CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 11 2011 254 267
56. A.G. Gilg, S.L. Tye, L.B. Tolliver, W.G. Wheeler, R.P. Visconti, J.D. Duncan, F.V. Kostova, L.N. Bolds, B.P. Toole, and B.L. Maria Targeting hyaluronan interactions in malignant gliomas and their drug-resistant multipotent progenitors Clin Cancer Res 14 2008 1804 1813