Breast cancer proteomics reveals correlation between estrogen receptor status and differential phosphorylation of PGRMC1

Breast Cancer Research

Volumn 10, Issue 5, 2008, Pages

  Neubauer, Hans ^a   Clare, Susan E ^a,b   Wozny, Wojciech ^c   Schwall, Gerhard P ^c   Poznanović, Slobodan ^c   Stegmann, Werner ^c   Vogel, Ulrich ^d   Sotlar, Karl ^d,e   Wallwiener, Diethelm ^a   Kurek, Raffael ^a,f   Fehm, Tanja ^a   Cahill, Michael A ^c,g  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PROTEOSYS AG   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e UNIVERSITY OF MUNICH   (Germany)

^f Merck Serono GmbH   (Germany)

^g CHARLES STURT UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AKT1 PROTEIN, HUMAN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; HYBRID PROTEIN; ISOPROTEIN; MEMBRANE PROTEIN; PGRMC1 PROTEIN, HUMAN; PHOSPHOSERINE; PROGESTERONE RECEPTOR; PROTEIN KINASE B; TUMOR PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BREAST TUMOR; COMPARATIVE STUDY; FEMALE; GENETICS; HUMAN; INTRADUCTAL CARCINOMA; LUNG CARCINOMA; METABOLISM; NEOPLASM; PAGET NIPPLE DISEASE; PATHOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS; TUMOR CELL LINE; TWO DIMENSIONAL GEL ELECTROPHORESIS; VALIDATION STUDY; WOUND HEALING;

AMINO ACID SUBSTITUTION; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CARCINOMA, LOBULAR; CELL LINE, TUMOR; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; HUMANS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; NEOPLASMS, HORMONE-DEPENDENT; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, PROGESTERONE; RECOMBINANT FUSION PROTEINS; WOUND HEALING;

EID: 59449107785     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2155     Document Type: Article

References (71)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin 2008, 58:71-96. 10.3322/CA.2007.0010, 18287387.
2. Fisher B, Jeong JH, Dignam J, Anderson S, Mamounas E, Wickerham DL, Wolmark N. Findings from recent National Surgical Adjuvant Breast and Bowel Project adjuvant studies in stage I breast cancer. J Natl Cancer Inst Monogr 2001, 30:62-66.
3. Osborne CK. Steroid hormone receptors in breast cancer management. Breast Cancer Res Treat 1998, 51:227-238. 10.1023/A:1006132427948, 10068081.
4. Henderson IC. Risk factors for breast cancer development. Cancer 1993, 71:2127-2140. 10.1002/1097-0142(19930315)71:6+<2127::AID-CNCR2820711602>3.0.CO;2-2, 8443762.
5. Howell A, Osborne CK, Morris C, Wakeling AE. ICI 182,780 (Faslodex): development of a novel, 'pure' antiestrogen. Cancer 2000, 89:817-825. 10.1002/1097-0142(20000815)89:4<817::AID-CNCR14>3.0.CO;2-6, 10951345.
6. McKeage K, Curran MP, Plosker GL. Fulvestrant: a review of its use in hormone receptor-positive metastatic breast cancer in postmenopausal women with disease progression following antiestrogen therapy. Drugs 2004, 64:633-648. 10.2165/00003495-200464060-00009, 15018596.
7. Platet N, Prevostel C, Derocq D, Joubert D, Rochefort H, Garcia M. Breast cancer cell invasiveness: correlation with protein kinase C activity and differential regulation by phorbol ester in estrogen receptor-positive and -negative cells. Int J Cancer 1998, 75:750-756. 10.1002/(SICI)1097-0215(19980302)75:5<750::AID-IJC14>3.0.CO;2-A, 9495244.
8. Thompson EW, Paik S, Brunner N, Sommers CL, Zugmaier G, Clarke R, Shima TB, Torri J, Donahue S, Lippman ME, Martin GR, Dickson RB. Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol 1992, 150:534-544. 10.1002/jcp.1041500314, 1537883.
9. Fuqua SA, Cui Y. Estrogen and progesterone receptor isoforms: clinical significance in breast cancer. Breast Cancer Res Treat 2004, 87(suppl 1):S3-10. 10.1007/s10549-004-1577-4, 15597215.
10. Price JE, Polyzos A, Zhang RD, Daniels LM. Tumorigenicity and metastasis of human breast carcinoma cell lines in nude mice. Cancer Res 1990, 50:717-721.
11. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lønning P, Børresen-Dale AL. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874. 58566, 11553815, 10.1073/pnas.191367098.
12. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lønning PE, Brown PO, Børresen-Dale AL, Botstein D. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 2003, 100:8418-8423. 166244, 12829800, 10.1073/pnas.0932692100.
13. Abd El-Rehim DM, Pinder SE, Paish CE, Bell J, Blamey RW, Robertson JF, Nicholson RI, Ellis IO. Expression of luminal and basal cytokeratins in human breast carcinoma. J Pathol 2004, 203:661-671. 10.1002/path.1559, 15141381.
14. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, Akslen LA, Ragaz J, Gown AM, Gilks CB, Rijn M, Perou CM. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004, 10:5367-5374. 10.1158/1078-0432.CCR-04-0220, 15328174.
15. Weigelt B, Glas AM, Wessels LF, Witteveen AT, Peterse JL, van't Veer LJ. Gene expression profiles of primary breast tumors maintained in distant metastases. Proc Natl Acad Sci USA 2003, 100:15901-15905. 307665, 14665696, 10.1073/pnas.2634067100.
16. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986, 315:1650-1659.
17. Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, Rijn M, Botstein D, Brown PO. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol 2004, 2:E7. 314300, 14737219, 10.1371/journal.pbio.0020007.
18. Poznanovic S, Wozny W, Schwall GP, Sastri C, Hunzinger C, Stegmann W, Schrattenholz A, Buchner A, Gangnus R, Burgemeister R, Cahill MA. Differential radioactive proteomic analysis of microdissected renal cell carcinoma tissue by 54 cm isoelectric focusing in serial immobilized pH gradient gels. J Proteome Res 2005, 4:2117-2125. 10.1021/pr050218q, 16335957.
19. Neubauer H, Clare SE, Kurek R, Fehm T, Wallwiener D, Sotlar K, Nordheim A, Wozny W, Schwall GP, Poznanoviæ S, Sastri C, Hunzinger C, Stegmann W, Schrattenholz A, Cahill MA. Breast cancer proteomics by laser capture microdissection, sample pooling, 54-cm IPG IEF, and differential iodine radioisotope detection. Electrophoresis 2006, 27:1840-1852. 10.1002/elps.200500739, 16645950.
20. Cahill MA. Progesterone receptor membrane component 1: an integrative review. J Steroid Biochem Mol Biol 2007, 105:16-36. 10.1016/j.jsbmb.2007.02.002, 17583495.
21. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567. 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2, 10612281.
22. Hand RA, Craven RJ. Hpr6.6 protein mediates cell death from oxidative damage in MCF-7 human breast cancer cells. J Cell Biochem 2003, 90:534-547. 10.1002/jcb.10648, 14523988.
23. Perou CM, Sørlie T, Eisen MB, Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature 2000, 406:747-752. 10.1038/35021093, 10963602.
24. van 't Veer LJ, Dai H, Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536. 10.1038/415530a, 11823860.
25. Gruvberger S, Ringner M, Chen Y, Panavally S, Saal LH, Borg A, Ferno M, Peterson C, Meltzer PS. Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res 2001, 61:5979-5984.
26. Velardo MJ, Burger C, Williams PR, Baker HV, Lopez MC, Mareci TH, White TE, Muzyczka N, Reier PJ. Patterns of gene expression reveal a temporally orchestrated wound healing response in the injured spinal cord. J Neurosci 2004, 24:8562-8576. 10.1523/JNEUROSCI.3316-04.2004, 15456830.
27. Bertucci F, Finetti P, Rougemont J, Charafe-Jauffret E, Cervera N, Tarpin C, Nguyen C, Xerri L, Houlgatte R, Jacquemier J, Viens P, Birnbaum D. Gene expression profiling identifies molecular subtypes of inflammatory breast cancer. Cancer Res 2005, 65:2170-2178. 10.1158/0008-5472.CAN-04-4115, 15781628.
28. Chang HY, Nuyten DS, Sneddon JB, Hastie T, Tibshirani R, Sørlie T, Dai H, He YD, van't Veer LJ, Bartelink H, Rijn M, Brown PO, Vijver MJ. Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc Natl Acad Sci USA 2005, 102:3738-3743. 548329, 15701700, 10.1073/pnas.0409462102.
29. Kang SK, So HH, Moon YS, Kim CH. Proteomic analysis of injured spinal cord tissue proteins using 2-DE and MALDI-TOF MS. Proteomics 2006, 6:2797-2812. 10.1002/pmic.200500621, 16586436.
30. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, Li J, Cohn MA, Cantley LC, Gygi SP. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci USA 2004, 101:12130-12135. 514446, 15302935, 10.1073/pnas.0404720101.
31. Sauer G, Korner R, Hanisch A, Ries A, Nigg EA, Sillje HH. Proteome analysis of the human mitotic spindle. Mol Cell Proteomics 2005, 4:35-43.
32. Suchanek M, Radzikowska A, Thiele C. Photo-leucine and photo-methionine allow identification of protein-protein interactions in living cells. Nat Methods 2005, 2:261-267. 10.1038/nmeth752, 15782218.
33. Airley RE, Mobasheri A. Hypoxic regulation of glucose transport, anaerobic metabolism and angiogenesis in cancer: novel pathways and targets for anticancer therapeutics. Chemotherapy 2007, 53:233-256. 10.1159/000104457, 17595539.
34. Crudden G, Loesel R, Craven RJ. Overexpression of the cytochrome p450 activator hpr6 (heme-1 domain protein/human progesterone receptor) in tumors. Tumour Biol 2005, 26:142-146. 10.1159/000086485, 15970648.
35. Hughes AL, Powell DW, Bard M, Eckstein J, Barbuch R, Link AJ, Espenshade PJ. Dap1/PGRMC1 binds and regulates cytochrome P450 enzymes. Cell Metab 2007, 5:143-149. 10.1016/j.cmet.2006.12.009, 17276356.
36. Sever N, Song BL, Yabe D, Goldstein JL, Brown MS, DeBose-Boyd RA. Insig-dependent ubiquitination and degradation of mammalian 3-hydroxy-3-methylglutaryl-CoA reductase stimulated by sterols and geranylgeraniol. J Biol Chem 2003, 278:52479-52490. 10.1074/jbc.M310053200, 14563840.
37. Brown AJ, Sun L, Feramisco JD, Brown MS, Goldstein JL. Cholesterol addition to ER membranes alters conformation of SCAP, the SREBP escort protein that regulates cholesterol metabolism. Mol Cell 2002, 10:237-245. 10.1016/S1097-2765(02)00591-9, 12191470.
38. Celis JE, Gromov P, Moreira JM, Cabezon T, Friis E, Vejborg IM, Proess G, Rank F, Gromova I. Apocrine cysts of the breast: biomarkers, origin, enlargement, and relation with cancer phenotype. Mol Cell Proteomics 2006, 5:462-483.
39. Rae FK, Martinez G, Gillinder KR, Smith A, Shooter G, Forrest AR, Grimmond SM, Little MH. Analysis of complementary expression profiles following WT1 induction versus repression reveals the cholesterol/fatty acid synthetic pathways as a possible major target of WT1. Oncogene 2004, 23:3067-3079. 10.1038/sj.onc.1207360, 15021918.
40. Wagner KD, Wagner N, Wellmann S, Schley G, Bondke A, Theres H, Scholz H. Oxygen-regulated expression of the Wilms' tumor suppressor Wt1 involves hypoxia-inducible factor-1 (HIF-1). Faseb J 2003, 17:1364-1366.
41. Helczynska K, Kronblad A, Jogi A, Nilsson E, Beckman S, Landberg G, Pahlman S. Hypoxia promotes a dedifferentiated phenotype in ductal breast carcinoma in situ. Cancer Res 2003, 63:1441-1444.
42. Gudjonsson T, Villadsen R, Nielsen HL, Ronnov-Jessen L, Bissell MJ, Petersen OW. Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev 2002, 16:693-706. 155359, 11914275, 10.1101/gad.952602.
43. Swiatek-De Lange M, Stampfl A, Hauck SM, Zischka H, Gloeckner CJ, Deeg CA, Ueffing M. Membrane-initiated effects of progesterone on calcium dependent signaling and activation of VEGF gene expression in retinal glial cells. Glia 2007, 55:1061-1073. 10.1002/glia.20523, 17551930.
44. Lee JN, Song B, DeBose-Boyd RA, Ye J. Sterol-regulated degradation of Insig-1 mediated by the membrane-bound ubiquitin ligase gp78. J Biol Chem 2006, 281:39308-39315. 10.1074/jbc.M608999200, 17043353.
45. Song BL, DeBose-Boyd RA. Ubiquitination of 3-hydroxy-3-methylglutaryl-CoA reductase in permeabilized cells mediated by cytosolic E1 and a putative membrane-bound ubiquitin ligase. J Biol Chem 2004, 279:28798-28806. 10.1074/jbc.M402442200, 15090540.
46. Page MJ, Amess B, Townsend RR, Parekh R, Herath A, Brusten L, Zvelebil MJ, Stein RC, Waterfield MD, Davies SC, O'Hare MJ. Proteomic definition of normal human luminal and myoepithelial breast cells purified from reduction mammoplasties. Proc Natl Acad Sci USA 1999, 96:12589-12594. 23001, 10535966, 10.1073/pnas.96.22.12589.
47. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer 2004, 4:665-676. 10.1038/nrc1431, 15343273.
48. Chu PG, Weiss LM. Keratin expression in human tissues and neoplasms. Histopathology 2002, 40:403-439. 10.1046/j.1365-2559.2002.01387.x, 12010363.
49. Boecker W, Buerger H. Evidence of progenitor cells of glandular and myoepithelial cell lineages in the human adult female breast epithelium: a new progenitor (adult stem) cell concept. Cell Prolif 2003, 36(suppl 1):73-84. 10.1046/j.1365-2184.36.s.1.7.x, 14521517.
50. Fan C, Oh DS, Wessels L, Weigelt B, Nuyten DS, Nobel AB, van't Veer LJ, Perou CM. Concordance among gene-expression-based predictors for breast cancer. N Engl J Med 2006, 355:560-569. 10.1056/NEJMoa052933, 16899776.
51. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995, 1:27-31. 10.1038/nm0195-27, 7584949.
52. Garvin S, Nilsson UW, Dabrosin C. Effects of oestradiol and tamoxifen on VEGF, soluble VEGFR-1, and VEGFR-2 in breast cancer and endothelial cells. Br J Cancer 2005, 93:1005-1010. 10.1038/sj.bjc.6602824, 16234819.
53. Ardelt AA, McCullough LD, Korach KS, Wang MM, Munzenmaier DH, Hurn PD. Estradiol regulates angiopoietin-1 mRNA expression through estrogen receptor-alpha in a rodent experimental stroke model. Stroke 2005, 36:337-341. 10.1161/01.STR.0000153795.38388.72, 15637314.
54. Gerner C, Steinkellner W, Holzmann K, Gsur A, Grimm R, Ensinger C, Obrist P, Sauermann G. Elevated plasma levels of crosslinked fibrinogen gamma-chain dimer indicate cancer-related fibrin deposition and fibrinolysis. Thromb Haemost 2001, 85:494-501.
55. Dvorak HF, Harvey VS, Estrella P, Brown LF, McDonagh J, Dvorak AM. Fibrin containing gels induce angiogenesis. Implications for tumor stroma generation and wound healing. Lab Invest 1987, 57:673-686.
56. Palumbo JS, Kombrinck KW, Drew AF, Grimes TS, Kiser JH, Degen JL, Bugge TH. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 2000, 96:3302-3309.
57. Moroz OV, Murzin AG, Makarova KS, Koonin EV, Wilson KS, Galperin MY. Dimeric dUTPases, HisE, and MazG belong to a new superfamily of all-alpha NTP pyrophosphohydrolases with potential 'house-cleaning' functions. J Mol Biol 2005, 347:243-255. 10.1016/j.jmb.2005.01.030, 15740738.
58. Peluso JJ, Pappalardo A, Losel R, Wehling M. Expression and function of PAIRBP1 within gonadotropin-primed immature rat ovaries: PAIRBP1 regulation of granulosa and luteal cell viability. Biol Reprod 2005, 73:261-270. 10.1095/biolreprod.105.041061, 15814896.
59. Engmann L, Losel R, Wehling M, Peluso JJ. Progesterone regulation of human granulosa/luteal cell viability by an RU486-independent mechanism. J Clin Endocrinol Metab 2006, 91:4962-4968. 10.1210/jc.2006-1128, 16984987.
60. Lemos TA, Passos DO, Nery FC, Kobarg J. Characterization of a new family of proteins that interact with the C-terminal region of the chromatin-remodeling factor CHD-3. FEBS Lett 2003, 533:14-20. 10.1016/S0014-5793(02)03737-7, 12505151.
61. Zhang H, Stephens LC, Kumar R. Metastasis tumor antigen family proteins during breast cancer progression and metastasis in a reliable mouse model for human breast cancer. Clin Cancer Res 2006, 12:1479-1486. 10.1158/1078-0432.CCR-05-1519, 16533771.
62. Leader JE, Wang C, Popov VM, Fu M, Pestell RG. Epigenetics and the estrogen receptor. Ann N Y Acad Sci 2006, 1089:73-87. 10.1196/annals.1386.047, 17261756.
63. Nguyen A, Cai H. Netrin-1 induces angiogenesis via a DCC-dependent ERK1/2-eNOS feed-forward mechanism. Proc Natl Acad Sci USA 2006, 103:6530-6535. 1458918, 16611730, 10.1073/pnas.0511011103.
64. Runko E, Kaprielian Z. Caenorhabditis elegans VEM-1, a novel membrane protein, regulates the guidance of ventral nerve cord-associated axons. J Neurosci 2004, 24:9015-9026. 10.1523/JNEUROSCI.2385-04.2004, 15483120.
65. Mehlen P, Furne C. Netrin-1: when a neuronal guidance cue turns out to be a regulator of tumorigenesis. Cell Mol Life Sci 2005, 62:2599-2616. 10.1007/s00018-005-5191-3, 16158190.
66. Bouchard JF, Moore SW, Tritsch NX, Roux PP, Shekarabi M, Barker PA, Kennedy TE. Protein kinase A activation promotes plasma membrane insertion of DCC from an intracellular pool: a novel mechanism regulating commissural axon extension. J Neurosci 2004, 24:3040-3050. 10.1523/JNEUROSCI.4934-03.2004, 15044543.
67. Krauss RS, Cole F, Gaio U, Takaesu G, Zhang W, Kang JS. Close encounters: regulation of vertebrate skeletal myogenesis by cell-cell contact. J Cell Sci 2005, 118:2355-2362. 10.1242/jcs.02397, 15923648.
68. Nikolopoulos SN, Giancotti FG. Netrin-integrin signaling in epithelial morphogenesis, axon guidance and vascular patterning. Cell Cycle 2005, 4:e131-135.
69. Slorach EM, Werb Z. Epithelial morphogenesis: Netrin comes to a sticky and terminal end. Curr Biol 2003, 13:R491-493. 10.1016/S0960-9822(03)00411-1, 12814570.
70. Strizzi L, Bianco C, Raafat A, Abdallah W, Chang C, Raafat D, Hirota M, Hamada S, Sun Y, Normanno N, Callahan R, Hinck L, Salomon D. Netrin-1 regulates invasion and migration of mouse mammary epithelial cells overexpressing Cripto-1 in vitro and in vivo. J Cell Sci 2005, 118:4633-4643. 10.1242/jcs.02574, 16176936.
71. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005, 17:548-558. 10.1016/j.ceb.2005.08.001, 16098727.