The basal epithelial marker P-cadherin associates with breast cancer cell populations harboring a glycolytic and acid-resistant phenotype

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Sousa, Bárbara ^a   Ribeiro, Ana S ^a   Nobre, Ana R ^a   Lopes, Nair ^a   Martins, Diana ^a   Pinheiro, Céline ^b,c   Vieira, André F ^a   Albergaria, André ^a,d   Gerhard, René ^a   Schmitt, Fernando ^a,d   Baltazar, Fátima ^b,c   Paredes, Joana ^a,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c UNIVERSITY OF MINHO   (Portugal)

^d University of Porto   (Portugal)

Author keywords

Breast cancer; Cancer stem cells; Hypoxia; P cadherin

Indexed keywords

CARBONATE DEHYDRATASE IX; CD147 ANTIGEN; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MONOCARBOXYLATE TRANSPORTER 1; P CADHERIN; SMALL INTERFERING RNA; CA9 PROTEIN, HUMAN; CADHERIN; CARBONATE DEHYDRATASE; CDH3 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; SLC2A1 PROTEIN, HUMAN; TUMOR ANTIGEN; TUMOR MARKER;

ARTICLE; BREAST CANCER; CAIX GENE; CANCER CELL; CELL HYPOXIA; CELL METABOLISM; CELL POPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE OVEREXPRESSION; GENE SILENCING; GLUT1 GENE; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; PHENOTYPE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; BREAST TUMOR; DISORDERS OF ACID BASE BALANCE; FEMALE; GENE EXPRESSION; GENETICS; METABOLISM; MULTICELLULAR SPHEROID; PAGET NIPPLE DISEASE; TISSUE MICROARRAY; TUMOR CELL LINE;

ACID-BASE IMBALANCE; ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CADHERINS; CARBONIC ANHYDRASES; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION; GLUCOSE TRANSPORTER TYPE 1; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; PHENOTYPE; SPHEROIDS, CELLULAR; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84908094892     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-734     Document Type: Article

References (58)

1. Yochim JM, Mitchell JA. Intrauterine Oxygen Tension in the Rat During Progestation: Its Possible Relation to Carbohydrate Metabolism and the Regulation of Nidation. Endocrinology 1968, 83:706-713. 10.1210/endo-83-4-706, 5685960.
2. Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell stem cell 2010, 7:150-161. 10.1016/j.stem.2010.07.007, 20682444.
3. Vacanti NM, Metallo CM. Exploring metabolic pathways that contribute to the stem cell phenotype. Biochim Biophys Acta 1830, 2013:2361-2369.
4. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012, 21:297-308. 10.1016/j.ccr.2012.02.014, 3311998, 22439925.
5. Birsoy K, Wang T, Possemato R, Yilmaz OH, Koch CE, Chen WW, Hutchins AW, Gultekin Y, Peterson TR, Carette JE, Brummelkamp TR, Clish CB, Sabatini DM. MCT1-mediated transport of a toxic molecule is an effective strategy for targeting glycolytic tumors. Nat Genet 2013, 45:104-108. 3530647, 23202129.
6. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3:721-732. 10.1038/nrc1187, 13130303.
7. Lundgren K, Holm C, Landberg G. Hypoxia and breast cancer: prognostic and therapeutic implications. Cell Mol Life Sci 2007, 64:3233-3247. 10.1007/s00018-007-7390-6, 17957335.
8. Chi JT, Wang Z, Nuyten DS, Rodriguez EH, Schaner ME, Salim A, Wang Y, Kristensen GB, Helland A, Borresen-Dale AL, Giaccia A, Longaker MT, Hastie T, Yang GP, van de Vijver MJ, Brown PO. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med 2006, 3:e47. 10.1371/journal.pmed.0030047, 1334226, 16417408.
9. Chen JL, Lucas JE, Schroeder T, Mori S, Wu J, Nevins J, Dewhirst M, West M, Chi JT. The genomic analysis of lactic acidosis and acidosis response in human cancers. PLoS Genet 2008, 4:e1000293. 10.1371/journal.pgen.1000293, 2585811, 19057672.
10. Gatza ML, Kung HN, Blackwell KL, Dewhirst MW, Marks JR, Chi JT. Analysis of tumor environmental response and oncogenic pathway activation identifies distinct basal and luminal features in HER2-related breast tumor subtypes. Breast Cancer Res 2011, 13:R62. 10.1186/bcr2899, 3218951, 21672245.
11. Chen CL, Chu JS, Su WC, Huang SC, Lee WY. Hypoxia and metabolic phenotypes during breast carcinogenesis: expression of HIF-1alpha, GLUT1, and CAIX. Virchows Arch 2010, 457:53-61. 10.1007/s00428-010-0938-0, 20526721.
12. Pinheiro C, Albergaria A, Paredes J, Sousa B, Dufloth R, Vieira D, Schmitt F, Baltazar F. Monocarboxylate transporter 1 is up-regulated in basal-like breast carcinoma. Histopathology 2010, 56:860-867. 10.1111/j.1365-2559.2010.03560.x, 20636790.
13. Pinheiro C, Sousa B, Albergaria A, Paredes J, Dufloth R, Vieira D, Schmitt F, Baltazar F. GLUT1 and CAIX expression profiles in breast cancer correlate with adverse prognostic factors and MCT1 overexpression. Histol Histopathol 2011, 26:1279-1286.
14. Tan EY, Yan M, Campo L, Han C, Takano E, Turley H, Candiloro I, Pezzella F, Gatter KC, Millar EK, O'Toole SA, McNeil CM, Crea P, Segara D, Sutherland RL, Harris AL, Fox SB. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br J Cancer 2009, 100:405-411. 10.1038/sj.bjc.6604844, 2634728, 19165203.
15. Dong C, Yuan T, Wu Y, Wang Y, Fan Teresa WM, Miriyala S, Lin Y, Yao J, Shi J, Kang T, Lorkiewicz P, St Clair D, Hung MC, Evers BM, Zhou BP. Loss of FBP1 by Snail-Mediated Repression Provides Metabolic Advantages in Basal-like Breast Cancer. Cancer Cell 2013, 23:316-331. 10.1016/j.ccr.2013.01.022, 3703516, 23453623.
16. McCleland ML, Adler AS, Shang Y, Hunsaker T, Truong T, Peterson D, Torres E, Li L, Haley B, Stephan JP, Belvin M, Hatzivassiliou G, Blackwood EM, Corson L, Evangelista M, Zha J, Firestein R. An integrated genomic screen identifies LDHB as an essential gene for triple-negative breast cancer. Cancer Res 2012, 72:5812-5823. 10.1158/0008-5472.CAN-12-1098, 23139210.
17. Koo HR, Park JS, Kang KW, Cho N, Chang JM, Bae MS, Kim WH, Lee SH, Kim MY, Kim JY, Seo M, Moon WK. 18 F-FDG uptake in breast cancer correlates with immunohistochemically defined subtypes. Eur Radiol 2014, 24:610-618. 10.1007/s00330-013-3037-1, 24097303.
18. Albergaria A, Ribeiro AS, Vieira AF, Sousa B, Nobre AR, Seruca R, Schmitt F, Paredes J. P-cadherin role in normal breast development and cancer. Int J Dev Biol 2011, 55:811-822. 10.1387/ijdb.113382aa, 22161837.
19. Radice GL, Ferreira-Cornwell MC, Robinson SD, Rayburn H, Chodosh LA, Takeichi M, Hynes RO. Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol 1997, 139:1025-1032. 10.1083/jcb.139.4.1025, 2139972, 9362520.
20. Kolle G, Ho M, Zhou Q, Chy HS, Krishnan K, Cloonan N, Bertoncello I, Laslett AL, Grimmond SM. Identification of human embryonic stem cell surface markers by combined membrane-polysome translation state array analysis and immunotranscriptional profiling. Stem Cells 2009, 27:2446-2456. 10.1002/stem.182, 19650036.
21. Daniel CW, Strickland P, Friedmann Y. Expression and functional role of E- and P-cadherins in mouse mammary ductal morphogenesis and growth. Develop Biol 1995, 169:511-519. 10.1006/dbio.1995.1165, 7781895.
22. Paredes J, Correia AL, Ribeiro AS, Albergaria A, Milanezi F, Schmitt FC. P-cadherin expression in breast cancer: a review. Breast Cancer Res 2007, 9:214. 10.1186/bcr1774, 2242663, 18001487.
23. Palacios J, Benito N, Pizarro A, Suarez A, Espada J, Cano A, Gamallo C. Anomalous expression of P-cadherin in breast carcinoma. Correlation with E-cadherin expression and pathological features. Am J Pathol 1995, 146:605-612. 1869170, 7534041.
24. Paredes J, Lopes N, Milanezi F, Schmitt FC. P-cadherin and cytokeratin 5: useful adjunct markers to distinguish basal-like ductal carcinomas in situ. Virchows Arch 2007, 450:73-80. 10.1007/s00428-006-0334-y, 17123107.
25. Paredes J, Albergaria A, Oliveira JT, Jeronimo C, Milanezi F, Schmitt FC. P-cadherin overexpression is an indicator of clinical outcome in invasive breast carcinomas and is associated with CDH3 promoter hypomethylation. Clin Cancer Res 2005, 11:5869-5877. 10.1158/1078-0432.CCR-05-0059, 16115928.
26. Paredes J, Milanezi F, Reis-Filho JS, Leitao D, Athanazio D, Schmitt F. Aberrant P-cadherin expression: is it associated with estrogen-independent growth in breast cancer?. Pathol Res Pract 2002, 198:795-801. 10.1078/0344-0338-00338, 12608656.
27. Sousa B, Paredes J, Milanezi F, Lopes N, Martins D, Dufloth R, Vieira D, Albergaria A, Veronese L, Carneiro V, Carvalho S, Costa JL, Zeferino L, Schmitt F. P-cadherin, vimentin and CK14 for identification of basal-like phenotype in breast carcinomas: an immunohistochemical study. Histol Histopathol 2010, 25:963-974.
28. Ribeiro AS, Albergaria A, Sousa B, Correia AL, Bracke M, Seruca R, Schmitt FC, Paredes J. Extracellular cleavage and shedding of P-cadherin: a mechanism underlying the invasive behaviour of breast cancer cells. Oncogene 2010, 29:392-402. 10.1038/onc.2009.338, 19901964.
29. Ribeiro AS, Sousa B, Carreto L, Mendes N, Nobre AR, Ricardo S, Albergaria A, Cameselle-Teijeiro JF, Gerhard R, Soderberg O, Seruca R, Santos MA, Schmitt F, Paredes J. P-cadherin functional role is dependent on E-cadherin cellular context: a proof of concept using the breast cancer model. J Pathol 2013, 229:705-718. 10.1002/path.4143, 23180380.
30. Vieira AF, Ricardo S, Ablett MP, Dionisio MR, Mendes N, Albergaria A, Farnie G, Gerhard R, Cameselle-Teijeiro JF, Seruca R, Schmitt F, Clarke RB, Paredes J. P-cadherin is coexpressed with CD44 and CD49f and mediates stem cell properties in basal-like breast cancer. Stem Cells 2012, 30:854-864. 10.1002/stem.1075, 22389315.
31. Feng W, Gentles A, Nair RV, Huang M, Lin Y, Lee CY, Cai S, Scheeren FA, Kuo AH, Diehn M. Targeting unique metabolic properties of breast tumor initiating cells. Stem Cells 2014, 32:1734-1745. 10.1002/stem.1662, 24497069.
32. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 98:1777-1785. 10.1093/jnci/djj495, 17179479.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
34. Messeguer X, Escudero R, Farre D, Nunez O, Martinez J, Alba MM. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 2002, 18:333-334. 10.1093/bioinformatics/18.2.333, 11847087.
35. Farre D, Roset R, Huerta M, Adsuara JE, Rosello L, Alba MM, Messeguer X. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 2003, 31:3651-3653. 10.1093/nar/gkg605, 169011, 12824386.
36. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, Gordon L, Hourlier T, Hunt S, Johnson N, Juettemann T, Kahari AK, Keenan S, Kulesha E, Martin FJ, Maurel T, McLaren WM, Murphy DN, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, et al. Ensembl 2014. Nucleic Acids Res 2014, 42:D749-D755. 10.1093/nar/gkt1196, 3964975, 24316576.
37. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CA, Ramalho-Santos J, Van Houten B, Schatten G. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 2011, 6:e20914. 10.1371/journal.pone.0020914, 3117868, 21698063.
38. Panopoulos AD, Yanes O, Ruiz S, Kida YS, Diep D, Tautenhahn R, Herrerias A, Batchelder EM, Plongthongkum N, Lutz M, Berggren WT, Zhang K, Evans RM, Siuzdak G, Izpisua, Belmonte JC. The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Res 2012, 22:168-177. 10.1038/cr.2011.177, 3252494,3252494, 22064701.
39. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, Dzeja PP, Ikeda Y, Perez-Terzic C, Terzic A. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 2011, 14:264-271. 10.1016/j.cmet.2011.06.011, 3156138, 21803296.
40. Generali D, Berruti A, Brizzi MP, Campo L, Bonardi S, Wigfield S, Bersiga A, Allevi G, Milani M, Aguggini S, Gandolfi V, Dogliotti L, Bottini A, Harris AL, Fox SB. Hypoxia-inducible factor-1alpha expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res 2006, 12:4562-4568. 10.1158/1078-0432.CCR-05-2690, 16899602.
41. Cooper C, Liu GY, Niu YL, Santos S, Murphy LC, Watson PH. Intermittent hypoxia induces proteasome-dependent down-regulation of estrogen receptor alpha in human breast carcinoma. Clin Cancer Res 2004, 10:8720-8727. 10.1158/1078-0432.CCR-04-1235, 15623657.
42. Paredes J, Stove C, Stove V, Milanezi F, Van Marck V, Derycke L, Mareel M, Bracke M, Schmitt F. P-cadherin is up-regulated by the antiestrogen ICI 182,780 and promotes invasion of human breast cancer cells. Cancer Res 2004, 64:8309-8317. 10.1158/0008-5472.CAN-04-0795, 15548699.
43. Gorski J, James C, Quinn J, Stewart G, Staunton K, Buckley N, McDyer F, Kennedy R, Wilson R, Mullan P, Harkin D. BRCA1 transcriptionally regulates genes associated with the basal-like phenotype in breast cancer. Breast Cancer Res Treat 2010, 122:721-731. 10.1007/s10549-009-0565-0, 19882246.
44. Lu Y, Chu A, Turker MS, Glazer PM. Hypoxia-induced epigenetic regulation and silencing of the BRCA1 promoter. Mol Cell Biol 2011, 31:3339-3350. 10.1128/MCB.01121-10, 3147797, 21670155.
45. Yan M, Rayoo M, Takano EA, Thorne H, Fox SB. BRCA1 tumours correlate with a HIF-1[alpha] phenotype and have a poor prognosis through modulation of hydroxylase enzyme profile expression. Br J Cancer 2009, 101:1168-1174. 10.1038/sj.bjc.6605287, 2768103, 19724277.
46. Arnes JB, Brunet JS, Stefansson I, Begin LR, Wong N, Chappuis PO, Akslen LA, Foulkes WD. Placental cadherin and the basal epithelial phenotype of BRCA1-related breast cancer. Clin Cancer Res 2005, 11:4003-4011. 10.1158/1078-0432.CCR-04-2064, 15930334.
47. Gest C, Joimel U, Huang L, Pritchard LL, Petit A, Dulong C, Buquet C, Hu CQ, Mirshahi P, Laurent M, Fauvel-Lafeve F, Cazin L, Vannier JP, Lu H, Soria J, Li H, Varin R, Soria C. Rac3 induces a molecular pathway triggering breast cancer cell aggressiveness: differences in MDA-MB-231 and MCF-7 breast cancer cell lines. BMC Cancer 2013, 13:63. 10.1186/1471-2407-13-63, 3576359, 23388133.
48. Swietach P, Vaughan-Jones RD, Harris AL. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev 2007, 26:299-310. 10.1007/s10555-007-9064-0, 17415526.
49. Gabison EE, Hoang-Xuan T, Mauviel A, Menashi S. EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair. Biochimie 2005, 87:361-368. 10.1016/j.biochi.2004.09.023, 15781323.
50. Zucker S, Hymowitz M, Rollo EE, Mann R, Conner CE, Cao J, Foda HD, Tompkins DC, Toole BP. Tumorigenic potential of extracellular matrix metalloproteinase inducer. Am J Pathol 2001, 158:1921-1928. 10.1016/S0002-9440(10)64660-3, 1891983, 11395366.
51. Ke X, Fei F, Chen Y, Xu L, Zhang Z, Huang Q, Zhang H, Yang H, Chen Z, Xing J. Hypoxia upregulates CD147 through a combined effect of HIF-1alpha and Sp1 to promote glycolysis and tumor progression in epithelial solid tumors. Carcinogenesis 2012, 33:1598-1607. 10.1093/carcin/bgs196, 22678117.
52. Schwab LP, Peacock DL, Majumdar D, Ingels JF, Jensen LC, Smith KD, Cushing RC, Seagroves TN. Hypoxia-inducible factor 1alpha promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res 2012, 14:R6. 10.1186/bcr3087, 3496121, 22225988.
53. Louie E, Nik S, Chen JS, Schmidt M, Song B, Pacson C, Chen XF, Park S, Ju J, Chen EI. Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation. Breast Cancer Res 2010, 12:R94. 10.1186/bcr2773, 3046435, 21067584.
54. Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, Clouthier SG, Wicha MS. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A 2012, 109:2784-2789. 10.1073/pnas.1018866109, 3286974, 22308314.
55. Oliveira-Costa JP, Zanetti JS, Silveira GG, Soave DF, Oliveira LR, Zorgetto VA, Soares FA, Zucoloto S, Ribeiro-Silva A. Differential expression of HIF-1alpha in CD44 + CD24-/low breast ductal carcinomas. Diagn Pathol 2011, 6:73. 10.1186/1746-1596-6-73, 3170242, 21824412.
56. Lock FE, McDonald PC, Lou Y, Serrano I, Chafe SC, Ostlund C, Aparicio S, Winum JY, Supuran CT, Dedhar S. Targeting carbonic anhydrase IX depletes breast cancer stem cells within the hypoxic niche. Oncogene 2013, 32:5210-5219. 10.1038/onc.2012.550, 23208505.
57. Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, Cameselle-Teijeiro JF, Milanezi F, Schmitt F, Paredes J. Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol 2011, 64:937-946. 10.1136/jcp.2011.090456, 21680574.
58. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, Clarke MF. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783. 10.1038/nature07733, 2778612, 19194462.