Mammary epithelial cells treated concurrently with TGF-α and TGF-β exhibit enhanced proliferation and death

Experimental Biology and Medicine

Volumn 232, Issue 8, 2007, Pages 1027-1040

  Casey, T M ^a,b   Mulvey, T M ^b   Patnode, T A ^b   Dean, A ^b   Zakrzewska, E ^b   Plaut, K ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Epithelial cell; Mammary; Transforming growth factor alpha (TGF ); Transforming growth factor beta (TGF )

Indexed keywords

FIBRONECTIN; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CELL CYCLE PROGRESSION; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DNA MICROARRAY; FLOW CYTOMETRY; GENE EXPRESSION; GROWTH RATE; MOUSE; NONHUMAN; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DEATH; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; FIBRONECTINS; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; MESODERM; MICE; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA;

EID: 34548454617     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0609-RM-218     Document Type: Article

References (81)

1. Todaro GJ, De Larco JE. Growth factors produced by sarcoma virus-transformed cells. Cancer Res 38:4147-4154, 1978.
2. Anzano MA, Roberts AB, Smith JM, Sporn MB, De Larco JE. Sarcoma growth factor from conditioned medium of virally transformed cells is composed of both type alpha and type beta transforming growth factors. Proc Natl Acad Sci U S A 80:6264-6268, 1983.
3. Roberts AB, Frolik CA, Anzano MA, Sporn MB. Transforming growth factors from neoplastic and nonneoplastic tissues. Fed Proc 42:2621-2626, 1983.
4. Amundadottir LT, Nass SJ, Berchem GJ, Johnson MD, Dickson RB. Cooperation of TGF alpha and c-Myc in mouse mammary tumorigenesis: coordinated stimulation of growth and suppression of apoptosis. Oncogene 13:757-765, 1996.
5. Daroqui MC, Puricelli LI, Urtreger AJ, Elizalde PV, Lanuza GM, Bal de Kier Joffe E. Involvement of TGF-beta(s)/T(beta)Rs system in tumor progression of murine mammary adenocarcinomas. Breast Cancer Res Treat 80:287-301, 2003.
6. de Jong JS, van Diest PJ, van der Valk P, Baak JP. Expression of growth factors, growth factor receptors and apoptosis related proteins in invasive breast cancer: relation to apoptotic rate. Breast Cancer Res Treat 66:201-208, 2001.
7. Gorska AE, Jensen RA, Shyr Y, Aakre ME, Bhowmick NA, Moses HL. Transgenic mice expressing a dominant-negative mutant type II transforming growth factor-beta receptor exhibit impaired mammary development and enhanced mammary tumor formation. Am J Pathol 163:1539-1549, 2003.
8. Muraoka RS, Koh Y, Roebuck LR, Sanders ME, Brantley-Sieders D, Gorska AE, Moses HL, Arteaga CL. Increased malignancy of Neu-induced mammary tumors overexpressing active transforming growth factor beta1. Mol Cell Biol 23:8691-8703, 2003.
9. Pilichowska M, Kimura N, Fujiwara H, Nagura H. Immunohistochemical study of TGF-alpha, TGF-beta1, EGFR, and IGF-1 expression in human breast carcinoma. Mod Pathol 10:969-975, 1997.
10. Rose-Hellekant TA, Sandgren EP. Transforming growth factor alpha- and c-myc-induced mammary carcinogenesis in transgenic mice. Oncogene 19:1092-1096, 2000.
11. Wakefield LM, Piek E, Bottinger EP. TGF-beta signaling in mammary gland development and tumorigenesis. J Mammary Gland Biol Neoplasia 6:67-82, 2001.
12. Smith GH, Sharp R, Kordon EC, Jhappan C, Merlino G. Transforming growth factor-alpha promotes mammary tumorigenesis through selective survival and growth of secretory epithelial cells. Am J Pathol 147:1081-1096, 1995.
13. Smith JA, Barraclough R, Fernig DG, Rudland PS. Identification of alpha transforming growth factor as a possible local trophic agent for the mammary gland. J Cell Physiol 141:362-370, 1989.
14. Zajchowski DA, Sager R. Induction of estrogen-regulated genes differs in immortal and tumorigenic human mammary epithelial cells expressing a recombinant estrogen receptor. Mol Endocrinol 5:1613-1623, 1991.
15. McGeady ML, Kerby S, Shankar V, Ciardiello F, Salomon D, Seidman M. Infection with a TGF-alpha retroviral vector transforms normal mouse mammary epithelial cells but not normal rat fibroblasts. Oncogene 4:1375-1382, 1989.
16. Shankar V, Ciardiello F, Kim N, Derynck R, Liscia DS, Merlo G, Langton BC, Sheer D, Callahan R, Bassin RH. Transformation of an established mouse mammary epithelial cell line following transfection with a human transforming growth factor alpha cDNA. Mol Carcinog 2:1-11, 1989.
17. Matsui Y, Halter SA, Holt JT, Hogan BL, Coffey RJ. Development of mammary hyperplasia and neoplasia in MMTV-TGF alpha transgenic mice. Cell 61:1147-1155, 1990.
18. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGF alpha overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 61:1137-1146, 1990.
19. Sandgren EP, Luetteke NC, Palmiter RD, Brinster RL, Lee DC. Overexpression of TGF alpha in transgenic mice: induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 61:1121-1135, 1990.
20. de Jong JS, van Diest PJ, Baak JP. Hot spot microvessel density and the mitotic activity index are strong additional prognostic indicators in invasive breast cancer. Histopathology 36:306-312, 2000.
21. Umekita Y, Enokizono N, Sagara Y, Kuriwaki K, Takasaki T, Yoshida A, Yoshida H. Immunohistochemical studies on oncogene products (EGF-R, c-erbB-2) and growth factors (EGF, TGF-alpha) in human breast cancer: their relationship to oestrogen receptor status, histological grade, mitotic index and nodal status. Virchows Arch A Pathol Anat Histopathol 420:345-351, 1992.
22. Albanell J, Baselga J. Trastuzumab, a humanized anti-HER2 monoclonal antibody, for the treatment of breast cancer. Drugs Today (Barc) 35:931-946, 1999.
23. Albanell J, Baselga J. The ErbB receptors as targets for breast cancer therapy. J Mammary Gland Biol Neoplasia 4:337-351, 1999.
24. Yeon CH, Pegram MD. Anti-erbB-2 antibody trastuzumab in the treatment of HER2-amplified breast cancer. Invest New Drugs 23:391-409, 2005.
25. Massague J, Cheifetz S, Ignotz RA, Boyd FT. Multiple type-beta transforming growth factors and their receptors. J Cell Physiol Suppl(Suppl 5):43-47, 1987.
26. Pierce DF Jr., Johnson MD, Matsui Y, Robinson SD, Gold LI, Purchio AF, Daniel CW, Hogan BL, Moses HL. Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGF-beta 1. Genes Dev 7:2308-2317, 1993.
27. Jhappan C, Geiser AG, Kordon EC, Bagheri D, Hennighausen L, Roberts AB, Smith GH, Merlino G. Targeting expression of a transforming growth factor beta 1 transgene to the pregnant mammary gland inhibits alveolar development and lactation. EMBO J 12:1835-1845, 1993.
28. Pierce DF Jr., Gorska AE, Chytil A, Meise KS, Page DL, Coffey RJ Jr., Moses HL. Mammary tumor suppression by transforming growth factor beta 1 transgene expression. Proc Natl Acad Sci U S A 92:4254-4258, 1995.
29. Forrester E, Chytil A, Bierie B, Aakre M, Gorska AE, Sharif-Afshar AR, Muller WJ, Moses HL. Effect of conditional knockout of the type II TGF-beta receptor gene in mammary epithelia on mammary gland development and polyomavirus middle T antigen induced tumor formation and metastasis. Cancer Res 65:2296-2302, 2005.
30. Miettinen PJ, Ebner R, Lopez AR, Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127:2021-2036, 1994.
31. Shook D, Keller R. Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech Dev 120:1351-1383, 2003.
32. Gilles C, Polette M, Piette J, Delvigne AC, Thompson EW, Foidart JM, Birembaut P. Vimentin expression in cervical carcinomas: association with invasive and migratory potential. J Pathol 180:175-180, 1996.
33. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442-454, 2002.
34. Muraoka-Cook RS, Dumont N, Arteaga CL. Dual role of transforming growth factor beta in mammary tumorigenesis and metastatic progression. Clin Cancer Res 11:937s-943s, 2005.
35. Chen CR, Kang Y, Massague J. Defective repression of c-myc in breast cancer cells: a loss at the core of the transforming growth factor beta growth arrest program. Proc Natl Acad Sci U S A 98:992-999, 2001.
36. Xie L, Law BK, Aakre ME, Edgerton M, Shyr Y, Bhowmick NA, Moses HL. Transforming growth factor beta-regulated gene expression in a mouse mammary gland epithelial cell line. Breast Cancer Res 5:R187-R198, 2003.
37. Hynes NE, Jaggi R, Kozma SC, Ball R, Muellener D, Wetherall NT, Davis BW, Groner B. New acceptor cell for transfected genomic DNA: oncogene transfer into a mouse mammary epithelial cell line. Mol Cell Biol 5:268-272, 1985.
38. Yosef H, Tamhane AC. Multiple Comparison Procedures. New York: John Wiley & Sons, 1987.
39. Van't Hof J. Cell Cycle Analysis. New York: Academic Press, 1973.
40. Freshney R. Culture of animal cells: A manual of basic technique. New York: Wiley-Liss, 1994.
41. Darzynkiewicz Z, Juan G, Li X, Gorczyca W, Murakami T, Traganos F. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27:1-20, 1997.
42. Sgonc R, Boeck G, Dietrich H, Gruber J, Recheis H, Wick G. Simultaneous determination of cell surface antigens and apoptosis. Trends Genet 10:41-42, 1994.
43. Plaut K, Maple RL. Characterization of binding of transforming growth factor-beta 1 to bovine mammary membranes. J Dairy Sci 78:1463-1469, 1995.
44. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25:169-193, 2000.
45. Okada M, Ohmura E, Kamiya Y, Murakami H, Onoda N, Iwashita M, Wakai K, Tsushima T, Shizume K. Transforming growth factor (TGF)-alpha in human milk. Life Sci 48:1151-1156, 1991.
46. Xu R, Doan QC, Regester GO. Detection and characterisation of transforming growth factor-beta in porcine colostrum. Biol Neonate 75:59-64, 1999.
47. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 110:673-687, 2002.
48. Giancotti FG, Ruoslahti E. Integrin Signaling. Science 285:1028-1033, 1999.
49. Sokol JP, Neil JR, Schiemann BJ, Schiemann WP. The use of cystatin C to inhibit epithelial-mesenchymal transition and morphological transformation stimulated by transforming growth factor-beta. Breast Cancer Res 7:R844-R853, 2005.
50. Sokol JP, Schiemann WP. Cystatin C antagonizes transforming growth factor beta signaling in normal and cancer cells. Mol Cancer Res 2:183-195, 2004.
51. Oft M, Heider KH, Beug H. TGFbeta signaling is necessary for carcinoma cell invasiveness and metastasis. Curr Biol 8:1243-1252, 1998.
52. Carcamo J, Zentella A, Massague J. Disruption of transforming growth factor beta signaling by a mutation that prevents transphosphorylation within the receptor complex. Mol Cell Biol 15:1573-1581, 1995.
53. Rodriguez C, Chen F, Weinberg RA, Lodish HF. Cooperative binding of transforming growth factor (TGF)-beta 2 to the types I and II TGF-beta receptors. J Biol Chem 270:15919-15922, 1995.
54. Dumont N, Arteaga CL. Transforming growth factor-beta and breast cancer: tumor promoting effects of transforming growth factor-beta. Breast Cancer Res 2:125-132, 2000.
55. Grunert S, Jechlinger M, Beug H. Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat Rev Mol Cell Biol 4:657-665, 2003.
56. Chen MS, Hurov J, White LS, Woodford-Thomas T, Piwnica-Worms H. Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol Cell Biol 21:3853-3861, 2001.
57. Chua SS, Ma Z, Ngan E, Tsai SY. Cdc25B as a steroid receptor coactivator. Vitam Horm 68:231-256, 2004.
58. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713, 1999.
59. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, McKeon F. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718, 1999.
60. Chepko G, Slack R, Carbott D, Khan S, Steadman L, Dickson RB. Differential alteration of stem and other cell populations in ducts and lobules of TGFalpha and c-Myc transgenic mouse mammary epithelium. Tissue Cell 37:393-412, 2005.
61. Assenmacher N, Hopfner KP. MRE11/RAD50/NBS1: complex activities. Chromosoma 113:157-166, 2004.
62. Lavin MF. The Mre11 complex and ATM: a two-way functional interaction in recognising and signaling DNA double strand breaks. DNA Repair (Amst) 3:1515-1520, 2004.
63. Liu S, Edgerton SM, Moore DH 2nd, Thor AD. Measures of cell turnover (proliferation and apoptosis) and their association with survival in breast cancer. Clin Cancer Res 7:1716-1723, 2001.
64. Archer CD, Parton M, Smith IE, Ellis PA, Salter J, Ashley S, Gui G, Sacks N, Ebbs SR, Allum W, Nasiri N, Dowsett M. Early changes in apoptosis and proliferation following primary chemotherapy for breast cancer. Br J Cancer 89:1035-1041, 2003.
65. Campiglio M, Locatelli A, Olgiati C, Normanno N, Somenzi G, Vigano L, Fumagalli M, Menard S, Gianni L. Inhibition of proliferation and induction of apoptosis in breast cancer cells by the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor ZD1839 ('Iressa') is independent of EGFR expression level. J Cell Physiol 198:259-268, 2004.
66. Chang J, Ormerod M, Powles TJ, Allred DC, Ashley SE, Dowsett M. Apoptosis and proliferation as predictors of chemotherapy response in patients with breast carcinoma. Cancer 89:2145-2152, 2000.
67. de Jong JS, van Diest PJ, Baak JP. Number of apoptotic cells as a prognostic marker in invasive breast cancer. Br J Cancer 82:368-373, 2000.
68. Mori I, Yang Q, Kakudo K. Predictive and prognostic markers for invasive breast cancer. Pathol Int 52:186-194, 2002.
69. Srinivas P, Abraham E, Ahamed I, Madhavan M, Vijayalakshmi NR, Nair MK, Balaram P. Apoptotic index: use in predicting recurrence in breast cancer patients. J Exp Clin Cancer Res 21:233-238, 2002.
70. Vakkala M, Lahteenmaki K, Raunio H, Paakko P, Soini Y. Apoptosis during breast carcinoma progression. Clin Cancer Res 5:319-324, 1999.
71. Zhu X, Di Y, Hu C, Wang Z. Expression of positive and negative regulators of cell cycle during wound healing. Chin Med J (Engl) 115:326-330, 2002.
72. Barnes DM, Gillett CE. Cyclin D1 in breast cancer. Breast Cancer Res Treat 52:1-15, 1998.
73. Vairo G, Livingston DM, Ginsberg D. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev 9:869-881, 1995.
74. Forrest A, Gabrielli B. Cdc25B activity is regulated by 14-3-3. Oncogene 20:4393-4401, 2001.
75. Gordon DM, Roof DM. Degradation of the kinesin Kip1p at anaphase onset is mediated by the anaphase-promoting complex and Cdc20p. Proc Natl Acad Sci U S A 98:12515-12520, 2001.
76. Choi KS, Eom YW, Kang Y, Ha MJ, Rhee H, Yoon JW, Kim SJ. Cdc2 and Cdk2 kinase activated by transforming growth factor-beta1 trigger apoptosis through the phosphorylation of retinoblastoma protein in FaO hepatoma cells. J Biol Chem 274:31775-31783, 1999.
77. D'Amours D, Jackson SP. The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 3:317-327, 2002.
78. Conaway RC, Brower CS, Conaway JW. Emerging roles of ubiquitin in transcription regulation. Science 296:1254-1258, 2002.
79. Dohn M, Zhang S, Chen X. p63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 20:3193-3205, 2001.
80. Kadakia M, Slader C, Berberich SJ. Regulation of p63 function by Mdm2 and MdmX. DNA Cell Biol 20:321-330, 2001.
81. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619, 1993.