Pregnancy-associated plasma protein A regulates mitosis and is epigenetically silenced in breast cancer

Journal of Pathology

Volumn 233, Issue 4, 2014, Pages 344-356

  Loddo, Marco ^a   Andryszkiewicz, Joanna ^a   Rodriguez Acebes, Sara ^a   Stoeber, Kai ^a   Jones, Allison ^b   Dafou, Dimitra ^b   Apostolidou, Sophia ^b   Wollenschlaeger, Alex ^a   Widschwendter, Martin ^b   Sainsbury, Richard ^a   Tudzarova, Slavica ^c   Williams, Gareth Haydn ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

breast cancer; cell cycle; epigenetic silencing; FoxM1; Foxo3a; IGF 1; MitoCheck; mitosis; PAPPA

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; PREGNANCY ASSOCIATED PLASMA PROTEIN A; SOMATOMEDIN C; TRANSCRIPTION FACTOR FOXM1; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CELL INVASION; CELL STRUCTURE; DNA METHYLATION; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOSIS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMETAPHASE; PROMOTER REGION; PROPHASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

BREAST CANCER; CELL CYCLE; EPIGENETIC SILENCING; FOXM1; FOXO3A; IGF-1; MITOCHECK; MITOSIS; PAPPA;

AGED; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE PROGRESSION; EPIGENOMICS; EPITHELIAL CELLS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MIDDLE AGED; MITOSIS; PHENOTYPE; PREGNANCY-ASSOCIATED PLASMA PROTEIN-A; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84904202489     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4393     Document Type: Article

References (39)

1. Neumann B, Walter T, Hériché JK, et al., Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 2010; 464: 721-727.
2. Walter T, Held M, Neumann B, et al., Automatic identification and clustering of chromosome phenotypes in a genome-wide RNAi screen by time-lapse imaging. J Struct Biol 2010; 170: 1-9.
3. Gisselsson D., Mitotic instability in cancer: is there method in the madness? Cell Cycle 2005; 4: 1007-1010.
4. Crosio C, Fimia GM, Loury R, et al., Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 2002; 22: 874-885.
5. Duregon E, Molinaro L, Volante M, et al., Comparative diagnostic and prognostic performances of the hematoxylin-eosin and phospho-histone H3 mitotic count and Ki-67 index in adrenocortical carcinoma. Mod Pathol 2014; doi: 10.1038/modpathol.2013.230.
6. Loddo M, Kingsbury SR, Rashid M, et al., Cell cycle-phase progression analysis identifies unique phenotypes of major prognostic and predictive significance in breast cancer. Br J Cancer 2009; 100: 959-970.
7. Rodriguez-Acebes S, Proctor I, Loddo M, et al., Targeting DNA replication before it starts: Cdc7 as a therapeutic target in p53-mutant breast cancers. Am J Pathol 2010; 177: 2034-2045.
8. Widschwendter M, Siegmund KD, Müller HM, et al., Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen. Cancer Res 2004; 64: 3807-3813.
9. Lenart P, Petronczki M, Steegmaier M, et al., The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol 2007; 17: 304-315.
10. Tudzarova S, Trotter MW, Wollenschlaeger A, et al., Molecular architecture of the DNA replication origin activation checkpoint. EMBO J 2010; 29: 3381-3394.
11. Rizki A, Mott JD, Bissell M.J., Polo-like kinase 1 is involved in invasion through extracellular matrix. Cancer Res 2007; 67: 11106-11110.
12. Vincourt JB, Etienne S, Cottet J, et al., C-propeptides of procollagens I α1 and αII that differentially accumulate in enchondromas versus chondrosarcomas regulate tumor cell survival and migration. Cancer Res 2010; 70: 4739-4748.
13. Kull FC Jr, Jacobs S, Su YF, et al., Monoclonal antibodies to receptors for insulin and somatomedin-C. J Biol Chem 1983; 258: 6561-6566.
14. Dumont N, Crawford YG, Sigaroudinia M, et al., Human mammary cancer progression model recapitulates methylation events associated with breast premalignancy. Breast Cancer Res 2009; 11: R87.
15. Lawrence JB, Oxvig C, Overgaard MT, et al., The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proc Natl Acad Sci USA 1999; 96: 3149-3153.
16. Laoukili J, Kooistra MR, Brás A, et al., FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 2005; 7: 126-136.
17. Delpuech O, Griffiths B, East P, et al., Induction of Mxi1-SRα by FOXO3a contributes to repression of Myc-dependent gene expression. Mol Cell Biol 2007; 27: 4917-4930.
18. McGovern UB, Francis RE, Peck B, et al., Gefitinib (Iressa) represses FOXM1 expression via FOXO3a in breast cancer. Mol Cancer Ther 2009; 8: 582-591.
19. Ma RY, Tong TH, Cheung AM, et al., Raf/MEK/MAPK signaling stimulates the nuclear translocation and transactivating activity of FOXM1c. J Cell Sci 2005; 118: 795-806.
20. Madureira PA, Varshochi R, Constantinidou D, et al., The Forkhead box M1 protein regulates the transcription of the estrogen receptor-α in breast cancer cells. J Biol Chem 2006; 281: 25167-25176.
21. Major ML, Lepe R, Costa RH,. Forkhead box M1B transcriptional activity requires binding of Cdk-cyclin complexes for phosphorylation-dependent recruitment of p300/CBP coactivators. Mol Cell Biol 2004; 24: 2649-2661.
22. Yang JY, Zong CS, Xia W, et al., ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 2008; 10: 138-148.
23. Boldt HB, Conover CA,. Pregnancy-associated plasma protein-A (PAPP-A): a local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Horm IGF Res 2007; 17: 10-18.
24. Conover CA,. Key questions and answers about pregnancy-associated plasma protein-A. Trends Endocrinol Metab 2012; 23: 242-249.
25. Kleinberg DL, Ruan W,. IGF-I, GH, and sex steroid effects in normal mammary gland development. J Mamm Gland Biol Neoplas 2008; 13: 353-360.
26. Sanchez-Calderon H, Rodriguez-de la Rosa L, Milo M, et al., RNA microarray analysis in prenatal mouse cochlea reveals novel IGF-I target genes: implication of MEF2 and FOXM1 transcription factors. PLoS One 2010; 5: e8699.
27. 2/M progression through mammalian target of rapamycin signaling in oligodendrocyte progenitors. Glia 2012; 60: 1684-1695.
28. 2/M-phase accumulation and apoptosis in multiple myeloma cells. Blood 2006; 107: 669-678.
29. Chen BK, Leiferman KM, Pittelkow MR, et al., Localization and regulation of pregnancy-associated plasma protein a expression in healing human skin. J Clin Endocrinol Metab 2003; 88: 4465-4471.
30. Tanner SJ, Hefferan TE, Rosen CJ, et al., Impact of pregnancy-associated plasma protein-a deletion on the adult murine skeleton. J Bone Miner Res 2008; 23: 655-662.
31. Mazerbourg S, Overgaard MT, Oxvig C, et al., Pregnancy-associated plasma protein-A (PAPP-A) in ovine, bovine, porcine, and equine ovarian follicles: involvement in IGF binding protein-4 proteolytic degradation and mRNA expression during follicular development. Endocrinology 2001; 142: 5243-5253.
32. Conover CA, Bale LK, Overgaard MT, et al., Metalloproteinase pregnancy-associated plasma protein A is a critical growth regulatory factor during fetal development. Development 2004; 131: 1187-1194.
33. Brambati B, Macintosh MC, Teisner B, et al., Low maternal serum levels of pregnancy associated plasma protein A (PAPP-A) in the first trimester in association with abnormal fetal karyotype. Br J Obstet Gynaecol 1993; 100: 324-326.
34. Conover CA, Bale LK,. Loss of pregnancy-associated plasma protein A extends lifespan in mice. Aging Cell 2007; 6: 727-729.
35. Boldt HB, Conover CA,. Overexpression of pregnancy-associated plasma protein-A in ovarian cancer cells promotes tumor growth in vivo. Endocrinology 2011; 152: 1470-1478.
36. Pan H, Hanada S, Zhao J, et al., Protein secretion is required for pregnancy-associated plasma protein-A to promote lung cancer growth in vivo. PLoS One 2012; 7: e48799.
37. Kuhajda FP, Eggleston JC,. Pregnancy-associated plasma protein A and extensive necrosis. Clinically significant predictors of early recurrence in stage I estrogen receptor-negative breast carcinoma. Lab Invest 1985; 53: 101-107.
38. Kuhajda FP, Eggleston JC,. Pregnancy-associated plasma protein A. A clinically significant predictor of early recurrence in stage I breast carcinoma is independent of estrogen receptor status. Am J Pathol 1985; 121: 342-348.
39. Callahan G, Denison SR, Phillips LA, et al., Characterization of the common fragile site FRA9E and its potential role in ovarian cancer. Oncogene 2003; 22: 590-601.