Role of the EphB2 receptor in autophagy, apoptosis and invasion in human breast cancer cells

Experimental Cell Research

Volumn 320, Issue 2, 2014, Pages 233-246

  Chukkapalli, Sahiti ^a   Amessou, Mohamed ^a   Dilly, Ashok K ^a   Dekhil, Hafedh ^b   Zhao, Jing ^c   Liu, Qiang ^c   Bejna, Alex ^a   Thomas, Ron D ^a   Bandyopadhyay, Sudeshna ^a   Bismar, Tarek A ^d   Neill, Daniel ^a   Azoulay, Laurent ^e   Batist, Gerald ^c,e   Kandouz, Mustapha ^a,f  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f WAYNE STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Autophagy; Breast cancer; EphB2; Ephrin; Invasion

Indexed keywords

AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 5; CASPASE 3; CASPASE 9; CYCLIC AMP DEPENDENT PROTEIN KINASE; EPHRIN RECEPTOR B2; GELATINASE A; GELATINASE B; LC3 PROTEIN; NEUTRALIZING ANTIBODY; PROTEIN; SMALL INTERFERING RNA; TUMOR MARKER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; BREAST CELL; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CONTROLLED STUDY; ENZYME REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE MICROARRAY; TUMOR INVASION;

APOPTOSIS; AUTOPHAGY; B-TYPE EPH RECEPTOR 2; BREAST CANCER; DOX; DOXYCYCLINE; EPHB2; EPHRIN; INVASION; MATRIX METALLOPROTEINASE; MMP; RECEPTOR TYROSINE KINASES; RTK; TISSUE MICROARRAY; TMA;

ANIMALS; APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CELLS, CULTURED; DISEASE PROGRESSION; FEMALE; HUMANS; MCF-7 CELLS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; RECEPTOR, EPHB2; TUMOR CELLS, CULTURED;

EID: 84890859460     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.10.022     Document Type: Article

References (77)

1. Arvanitis D., Davy A. Eph/Ephrin signaling: networks. Genes Dev. 2008, 22:416-429.
2. Bacus S., Flowers J.L., Press M.F., Bacus J.W., McCarty K.S. The evaluation of estrogen receptor in primary breast carcinoma by computer-assisted image analysis. Am. J. Clin. Pathol. 1988, 90:233-239.
3. Baehrecke E.H. Autophagy: dual roles in life and death?. Nat. Rev. Mol. Cell Biol. 2005, 6:505-510.
4. Batlle E., Bacani J., Begthel H., Jonkheer S., Gregorieff A., van de B.M., Malats N., Sancho E., Boon E., Pawson T., Gallinger S., Pals S., Clevers H. EphB receptor activity suppresses colorectal cancer progression. Nature 2005, 435:1126-1130.
5. Berclaz G., Flutsch B., Altermatt H.J., Rohrbach V., Djonov V., Ziemiecki A., Dreher E., Andres A.C. Loss of EphB4 receptor tyrosine kinase protein expression during carcinogenesis of the human breast. Oncol. Rep. 2002, 9:985-989.
6. Bhushan L., Kandpal R.P. EphB6 receptor modulates micro RNA profile of breast carcinoma cells. PLoS One 2011, 6:e22484.
7. Brantley-Sieders M., Jiang A., Sarma K., Badu-Nkansah A., Walter D.L., Shyr Y., Chen J. Eph/Ephrin profiling in human breast cancer reveals significant associations between expression level and clinical outcome. PLoS One 2011, 6:e24426.
8. Brantley-Sieders D.M., Zhuang G., Hicks D., Fang W.B., Hwang Y., Cates J.M., Coffman K., Jackson D., Bruckheimer E., Muraoka-Cook R.S., Chen J. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J. Clin. Invest. 2008, 118:64-78.
9. Chambers A.F. MDA-MB-435 and M14 cell lines: identical but not M14 melanoma?. Cancer Res. 2009, 69:5292-5293.
10. Chen Y., Fu A.K., Ip N.Y. Eph receptors at synapses: implications in neurodegenerative diseases. Cell Signal. 2012, 24:606-611.
11. Chunder N., Mandal S., Basu D., Roy A., Roychoudhury S., Panda C.K. Deletion mapping of chromosome 1 in early onset and late onset breast tumors-a comparative study in eastern India. Pathol. Res. Pract. 2003, 199:313-321.
12. Dalby K.N., Tekedereli I., Lopez-Berestein G., Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 2010, 6:322-329.
13. Debnath J. The multifaceted roles of autophagy in tumors-implications for breast cancer. J. Mammary Gland Biol. Neoplasia 2011, 16:173-187.
14. Dodelet V.C., Pasquale E.B. Eph receptors and Ephrin ligands: embryogenesis to tumorigenesis. Oncogene 2000, 19:5614-5619.
15. Ellison G., Klinowska T., Westwood R.F., Docter E., French T., Fox J.C. Further evidence to support the melanocytic origin of MDA-MB-435. Mol. Pathol. 2002, 55:294-299.
16. Espina V., Mariani B.D., Gallagher R.I., Tran K., Banks S., Wiedemann J., Huryk H., Mueller C., Adamo L., Deng J., Petricoin E.F., Pastore L., Zaman S., Menezes G., Mize J., Johal J., Edmiston K., Liotta L.A. Malignant precursor cells pre-exist in human breast DCIS and require autophagy for survival. PLoS One 2010, 5:e10240.
17. Fang W.B., Brantley-Sieders D.M., Parker M.A., Reith A.D., Chen J. A kinase-dependent role for EphA2 receptor in promoting tumor growth and metastasis. Oncogene 2005, 24:7859-7868.
18. Fimia G.M., Piacentini M. Regulation of autophagy in mammals and its interplay with apoptosis. Cell Mol. Life Sci. 2010, 67:1581-1588.
19. Flanagan J.G., Vanderhaeghen P. The Ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 1998, 21:309-345.
20. Flenniken A.M., Gale N.W., Yancopoulos G.D., Wilkinson D.G. Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev. Biol. 1996, 179:382-401.
21. Friedman G.C., O'Leary D.D. Eph receptor tyrosine kinases and their ligands in neural development. Curr. Opin. Neurobiol. 1996, 6:127-133.
22. Frisen J., Holmberg J., Barbacid M. Ephrins and their Eph receptors: multitalented directors of embryonic development. EMBO J. 1999, 18:5159-5165.
23. Gale N.W., Holland S.J., Valenzuela D.M., Flenniken A., Pan L., Ryan T.E., Henkemeyer M., Strebhardt K., Hirai H., Wilkinson D.G., Pawson T., Davis S., Yancopoulos G.D. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 1996, 17:9-19.
24. Garber K. Of Ephs and Ephrins: companies target guidance molecules in cancer. J. Natl. Cancer Inst. 2010, 102:1692-1694.
25. Genander M., Halford M.M., Xu N.J., Eriksson M., Yu Z., Qiu Z., Martling A., Greicius G., Thakar S., Catchpole T., Chumley M.J., Zdunek S., Wang C., Holm T., Goff S.P., Pettersson S., Pestell R.G., Henkemeyer M., Frisen J. Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell 2009, 139:679-692.
26. Guo D.L., Zhang J., Yuen S.T., Tsui W.Y., Chan A.S., Ho C., Ji J., Leung S.Y., Chen X. Reduced expression of EphB2 that parallels invasion and metastasis in colorectal tumours. Carcinogenesis 2006, 27:454-464.
27. Harburg G.C., Hinck L. Navigating breast cancer: axon guidance molecules as breast cancer tumor suppressors and oncogenes. J. Mammary Gland Biol. Neoplasia 2011, 16:257-270.
28. He L., Hristova K. Physical-chemical principles underlying RTK activation, and their implications for human disease. Biochim. Biophys. Acta 2012, 1818:995-1005.
29. Himanen J.P., Chumley M.J., Lackmann M., Li C., Barton W.A., Jeffrey P.D., Vearing C., Geleick D., Feldheim D.A., Boyd A.W., Henkemeyer M., Nikolov D.B. Repelling class discrimination: Ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 2004, 7:501-509.
30. Hiramoto-Yamaki N., Takeuchi S., Ueda S., Harada K., Fujimoto S., Negishi M., Katoh H. Ephexin4 and EphA2 mediate cell migration through a RhoG-dependent mechanism. J. Cell Biol. 2010, 190:461-477.
31. Holder N., Klein R. Eph receptors and Ephrins: effectors of morphogenesis. Development 1999, 126:2033-2044.
32. Hollestelle A., Nagel J.H., Smid M., Lam S., Elstrodt F., Wasielewski M., Ng S.S., French P.J., Peeters J.K., Rozendaal M.J., Riaz M., Koopman D.G., Ten Hagen T.L., de Leeuw B.H., Zwarthoff E.C., Teunisse A., van der Spek P.J., Klijn J.G., Dinjens W.N., Ethier S.P., Clevers H., Jochemsen A.G., den Bakker M.A., Foekens J.A., Martens J.W., Schutte M. Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res. Treat. 2010, 121:53-64.
33. Hollestelle A., Schutte M. Comment Re: MDA-MB-435 and M14 cell lines: identical but not M14 Melanoma?. Cancer Res. 2009, 69:7893.
34. Holmberg J., Genander M., Halford M.M., Anneren C., Sondell M., Chumley M.J., Silvany R.E., Henkemeyer M., Frisen J. EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell 2006, 125:1151-1163.
35. Hruska M., Dalva M.B. Ephrin regulation of synapse formation, function and plasticity. Mol. Cell Neurosci. 2012, 50:35-44.
36. Huusko P., Ponciano-Jackson D., Wolf M., Kiefer J.A., Azorsa D.O., Tuzmen S., Weaver D., Robbins C., Moses T., Allinen M., Hautaniemi S., Chen Y., Elkahloun A., Basik M., Bova G.S., Bubendorf L., Lugli A., Sauter G., Schleutker J., Ozcelik H., Elowe S., Pawson T., Trent J.M., Carpten J.D., Kallioniemi O.P., Mousses S. Nonsense-mediated decay microarray analysis identifies mutations of EPHB2 in human prostate cancer. Nat. Genet. 2004, 36:979-983.
37. Jubb A.M., Zhong F., Bheddah S., Grabsch H.I., Frantz G.D., Mueller W., Kavi V., Quirke P., Polakis P., Koeppen H. EphB2 is a prognostic factor in colorectal cancer. Clin. Cancer Res. 2005, 11:5181-5187.
38. Kaenel P., Mosimann M., Andres A.C. The multifaceted roles of Eph-Ephrin signaling in breast cancer. Cell Adhes. Migr. 2012, 6:138-147.
39. Kandouz M. The Eph/Ephrin family in cancer metastasis: communication at the service of invasion. Cancer Metastasis Rev. 2012, 31:353-373.
40. Kandouz M., Haidara K., Zhao J., Brisson M.L., Batist G. The EphB2 tumor suppressor induces autophagic cell death via concomitant activation of the ERK1/2 and PI3K pathways. Cell Cycle 2010, 9:398-407.
41. Kimmelman A.C. The dynamic nature of autophagy in cancer. Genes Dev. 2011, 25:1999-2010.
42. Kittles R.A., Baffoe-Bonnie A.B., Moses T.Y., Robbins C.M., Ahaghotu C., Huusko P., Pettaway C., Vijayakumar S., Bennett J., Hoke G., Mason T., Weinrich S., Trent J.M., Collins F.S., Mousses S., Bailey-Wilson J., Furbert-Harris P., Dunston G., Powell I.J., Carpten J.D. A common nonsense mutation in EphB2 is associated with prostate cancer risk in African American men with a positive family history. J. Med. Genet. 2006, 43:507-511.
43. Klein R. Bidirectional modulation of synaptic functions by Eph/Ephrin signaling. Nat. Neurosci. 2009, 12:15-20.
44. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 2008, 9:1004-1010.
45. Kumar S.R., Singh J., Xia G., Krasnoperov V., Hassanieh L., Ley E.J., Scehnet J., Kumar N.G., Hawes D., Press M.F., Weaver F.A., Gill P.S. Receptor tyrosine kinase EphB4 is a survival factor in breast cancer. Am. J. Pathol. 2006, 169:279-293.
46. Lu M., Miller K.D., Gokmen-Polar Y., Jeng M.H., Kinch M.S. EphA2 overexpression decreases estrogen dependence and tamoxifen sensitivity. Cancer Res. 2003, 63:3425-3429.
47. Lugli A., Spichtin H., Maurer R., Mirlacher M., Kiefer J., Huusko P., Azorsa D., Terracciano L., Sauter G., Kallioniemi O.P., Mousses S., Tornillo L. EphB2 expression across 138 human tumor types in a tissue microarray: high levels of expression in gastrointestinal cancers. Clin. Cancer Res. 2005, 11:6450-6458.
48. Luo S., Rubinsztein D.C. Atg5 and Bcl-2 provide novel insights into the interplay between apoptosis and autophagy. Cell Death Differ. 2007, 14:1247-1250.
49. McClelland R.A., Berger U., Miller L.S., Powles T.J., Jensen E.V., Coombes R.C. Immunocytochemical assay for estrogen receptor: relationship to outcome of therapy in patients with advanced breast cancer. Cancer Res. 1986, 46:4241s-4243s.
50. Merlos-Suarez A., Batlle E. Eph-Ephrin signalling in adult tissues and cancer. Curr. Opin. Cell Biol. 2008, 20:194-200.
51. Montel V., Suzuki M., Galloy C., Mose E.S., Tarin D. Expression of melanocyte-related genes in human breast cancer and its implications. Differentiation 2009, 78:283-291.
52. Nakada M., Niska J.A., Miyamori H., McDonough W.S., Wu J., Sato H., Berens M.E. The phosphorylation of EphB2 receptor regulates migration and invasion of human glioma cells. Cancer Res. 2004, 64:3179-3185.
53. Nakada M., Niska J.A., Tran N.L., McDonough W.S., Berens M.E. EphB2/R-Ras signaling regulates glioma cell adhesion, growth, and invasion. Am. J. Pathol. 2005, 167:565-576.
54. Nievergall E., Saunders T., Lackmann M. Targeting of EPH receptor tyrosine kinases for anticancer therapy. Crit. Rev.Oncog. 2012, 17:211-232.
55. Noren N.K., Foos G., Hauser C.A., Pasquale E.B. The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat. Cell Biol. 2006, 8:815-825.
56. Noren N.K., Lu M., Freeman A.L., Koolpe M., Pasquale E.B. Interplay between EphB4 on tumor cells and vascular Ephrin-B2 regulates tumor growth. Proc. Natl. Acad. Sci. USA 2004, 101:5583-5588.
57. Noren N.K., Lu M., Freeman A.L., Koolpe M., Pasquale E.B. Interplay between EphB4 on tumor cells and vascular Ephrin-B2 regulates tumor growth. Proc. Natl. Acad. Sci. USA 2004, 101:5583-5588.
58. O'Leary D.D., Wilkinson D.G. Eph receptors and Ephrins in neural development. Curr. Opin. Neurobiol. 1999, 9:65-73.
59. Oshima T., Akaike M., Yoshihara K., Shiozawa M., Yamamoto N., Sato T., Akihito N., Nagano Y., Fujii S., Kunisaki C., Wada N., Rino Y., Tanaka K., Masuda M., Imada T. Overexpression of EphA4 gene and reduced expression of EphB2 gene correlates with liver metastasis in colorectal cancer. Int. J. Oncol. 2008, 33:573-577.
60. Pasquale E.B. Eph-Ephrin bidirectional signaling in physiology and disease. Cell 2008, 133:38-52.
61. Rae J.M., Creighton C.J., Meck J.M., Haddad B.R., Johnson M.D. MDA-MB-435 cells are derived from M14 melanoma cells-a loss for breast cancer, but a boon for melanoma research. Breast Cancer Res.Treat. 2007, 104:13-19.
62. Ragnarsson G., Eiriksdottir G., Johannsdottir J.T., Jonasson J.G., Egilsson V., Ingvarsson S. Loss of heterozygosity at chromosome 1p in different solid human tumours: association with survival. Br. J. Cancer 1999, 79:1468-1474.
63. Rikiishi H. Novel insights into the interplay between apoptosis and autophagy. Int. J. Cell Biol. 2012, 2012:317645.
64. Ross D.T., Scherf U., Eisen M.B., Perou C.M., Rees C., Spellman P., Iyer V., Jeffrey S.S., Van de Rijn M., Waltham M., Pergamenschikov A., Lee J.C., Lashkari D., Shalon D., Myers T.G., Weinstein J.N., Botstein D., Brown P.O. Systematic variation in gene expression patterns in human cancer cell lines. Nat. Genet. 2000, 24:227-235.
65. Scarlatti F., Granata R., Meijer A.J., Codogno P. Does autophagy have a license to kill mammalian cells?. Cell Death Differ. 2009, 16:12-20.
66. Sellappan S., Grijalva R., Zhou X., Yang W., Eli M.B., Mills G.B., Yu D. Lineage infidelity of MDA-MB-435 cells: expression of melanocyte proteins in a breast cancer cell line. Cancer Res. 2004, 64:3479-3485.
67. Tan E.Y., Campo L., Han C., Turley H., Pezzella F., Gatter K.C., Harris A.L., Fox S.B. BNIP3 as a progression marker in primary human breast cancer; opposing functions in in situ versus invasive cancer. Clin. Cancer Res. 2007, 13:467-474.
68. Truitt L., Freywald T., DeCoteau J., Sharfe N., Freywald A. The EphB6 receptor cooperates with c-Cbl to regulate the behavior of breast cancer cells. Cancer Res. 2010, 70:1141-1153.
69. Ustach C.V., Taube M.E., Hurst N.J., Bhagat S., Bonfil R.D., Cher M.L., Schuger L., Kim H.R. A potential oncogenic activity of platelet-derived growth factor d in prostate cancer progression. Cancer Res. 2004, 64:1722-1729.
70. Wang H.U., Chen Z.F., Anderson D.J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by Ephrin-B2 and its receptor Eph-B4. Cell 1998, 93:741-753.
71. Wang S.D., Rath P., Lal B., Richard J.P., Li Y., Goodwin C.R., Laterra J., Xia S. EphB2 receptor controls proliferation/migration dichotomy of glioblastoma by interacting with focal adhesion kinase. Oncogene 2012, 31:5132-5143.
72. Wu Q., Suo Z., Risberg B., Karlsson M.G., Villman K., Nesland J.M. Expression of Ephb2 and Ephb4 in breast carcinoma. Pathol. Oncol. Res. 2004, 10:26-33.
73. Wu W.K., Coffelt S.B., Cho C.H., Wang X.J., Lee C.W., Chan F.K., Yu J., Sung J.J. The autophagic paradox in cancer therapy. Oncogene 2012, 31:939-953.
74. Yancopoulos G.D., Klagsbrun M., Folkman J. Vasculogenesis, angiogenesis, and growth factors: Ephrins enter the fray at the border. Cell 1998, 93:661-664.
75. Yang N.Y., Pasquale E.B., Owen L.B., Ethell I.M. The EphB4 receptor-tyrosine kinase promotes the migration of melanoma cells through Rho-mediated actin cytoskeleton reorganization. J. Biol. Chem. 2006, 281:32574-32586.
76. Yang Z.J., Chee C.E., Huang S., Sinicrope F.A. The role of autophagy in cancer: therapeutic implications. Mol. Cancer Ther. 2011, 10:1533-1541.
77. Zelinski D.P., Zantek N.D., Stewart J.C., Irizarry A.R., Kinch M.S. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 2001, 61:2301-2306.