Skip to main content
Top
Published in: Breast Cancer Research 1/2014

Open Access 01-02-2014 | Research article

Parity-related molecular signatures and breast cancer subtypes by estrogen receptor status

Authors: Melissa Rotunno, Xuezheng Sun, Jonine Figueroa, Mark E Sherman, Montserrat Garcia-Closas, Paul Meltzer, Tyisha Williams, Sallie Smith Schneider, D Joseph Jerry, Xiaohong R Yang, Melissa A Troester

Published in: Breast Cancer Research | Issue 1/2014

Login to get access

Abstract

Introduction

Relationships of parity with breast cancer risk are complex. Parity is associated with decreased risk of postmenopausal hormone receptor–positive breast tumors, but may increase risk for basal-like breast cancers and early-onset tumors. Characterizing parity-related gene expression patterns in normal breast and breast tumor tissues may improve understanding of the biological mechanisms underlying this complex pattern of risk.

Methods

We developed a parity signature by analyzing microRNA microarray data from 130 reduction mammoplasty (RM) patients (54 nulliparous and 76 parous). This parity signature, together with published parity signatures, was evaluated in gene expression data from 150 paired tumors and adjacent benign breast tissues from the Polish Breast Cancer Study, both overall and by tumor estrogen receptor (ER) status.

Results

We identified 251 genes significantly upregulated by parity status in RM patients (parous versus nulliparous; false discovery rate = 0.008), including genes in immune, inflammation and wound response pathways. This parity signature was significantly enriched in normal and tumor tissues of parous breast cancer patients, specifically in ER-positive tumors.

Conclusions

Our data corroborate epidemiologic data, suggesting that the etiology and pathogenesis of breast cancers vary by ER status, which may have implications for developing prevention strategies for these tumors.
Appendix
Available only for authorised users
Literature
2.
go back to reference Lambe M, Hsieh C, Trichopoulos D, Ekbom A, Pavia M, Adami HO: Transient increase in the risk of breast cancer after giving birth. N Engl J Med. 1994, 331: 5-9.CrossRefPubMed Lambe M, Hsieh C, Trichopoulos D, Ekbom A, Pavia M, Adami HO: Transient increase in the risk of breast cancer after giving birth. N Engl J Med. 1994, 331: 5-9.CrossRefPubMed
3.
go back to reference Jatoi I, Anderson WF: Qualitative age interactions in breast cancer studies: a mini-review. Future Oncol. 2010, 6: 1781-1788.CrossRefPubMed Jatoi I, Anderson WF: Qualitative age interactions in breast cancer studies: a mini-review. Future Oncol. 2010, 6: 1781-1788.CrossRefPubMed
4.
go back to reference O’Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, Man YG, Borges V, Schedin P: Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol. 2010, 176: 1241-1255.CrossRefPubMedPubMedCentral O’Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, Man YG, Borges V, Schedin P: Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol. 2010, 176: 1241-1255.CrossRefPubMedPubMedCentral
5.
go back to reference Schedin P, O’Brien J, Rudolph M, Stein T, Borges V: Microenvironment of the involuting mammary gland mediates mammary cancer progression. J Mammary Gland Biol Neoplasia. 2007, 12: 71-82.CrossRefPubMed Schedin P, O’Brien J, Rudolph M, Stein T, Borges V: Microenvironment of the involuting mammary gland mediates mammary cancer progression. J Mammary Gland Biol Neoplasia. 2007, 12: 71-82.CrossRefPubMed
6.
go back to reference Albrektsen G, Heuch I, Hansen S, Kvåle G: Breast cancer risk by age at birth, time since birth and time intervals between births: Exploring interaction effects. Br J Cancer. 2005, 92: 167-175.CrossRefPubMed Albrektsen G, Heuch I, Hansen S, Kvåle G: Breast cancer risk by age at birth, time since birth and time intervals between births: Exploring interaction effects. Br J Cancer. 2005, 92: 167-175.CrossRefPubMed
7.
go back to reference Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME: Etiology of hormone receptor-defined breast cancer: A systematic review of the literature. Cancer Epidemiol Biomarkers Prev. 2004, 13: 1558-1568.PubMed Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME: Etiology of hormone receptor-defined breast cancer: A systematic review of the literature. Cancer Epidemiol Biomarkers Prev. 2004, 13: 1558-1568.PubMed
8.
go back to reference Ma H, Bernstein L, Pike MC, Ursin G: Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res. 2006, 8: R43-CrossRefPubMedPubMedCentral Ma H, Bernstein L, Pike MC, Ursin G: Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res. 2006, 8: R43-CrossRefPubMedPubMedCentral
9.
go back to reference Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A, Fasching PA, Hein R, Spurdle AB, Blows F, Driver K, Flesch-Janys D, Heinz J, Sinn P, Vrieling A, Heikkinen T, Aittomäki K, Heikkilä P, Blomqvist C, Lissowska J, Peplonska B, Chanock S, Figueroa J, Brinton L, Hall P, Czene K, et al: Associations of breast cancer risk factors with tumor subtypes: A pooled analysis from the Breast Cancer Association Consortium Studies. J Natl Cancer Inst. 2011, 103: 250-263.CrossRefPubMed Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A, Fasching PA, Hein R, Spurdle AB, Blows F, Driver K, Flesch-Janys D, Heinz J, Sinn P, Vrieling A, Heikkinen T, Aittomäki K, Heikkilä P, Blomqvist C, Lissowska J, Peplonska B, Chanock S, Figueroa J, Brinton L, Hall P, Czene K, et al: Associations of breast cancer risk factors with tumor subtypes: A pooled analysis from the Breast Cancer Association Consortium Studies. J Natl Cancer Inst. 2011, 103: 250-263.CrossRefPubMed
10.
go back to reference Faupel-Badger JM, Arcaro KF, Balkam JJ, Eliassen AH, Hassiotou F, Lebrilla CB, Michels KB, Palmer JR, Schedin P, Stuebe AM, Watson CJ, Sherman ME: Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute–sponsored workshop. J Natl Cancer Inst. 2013, 105: 166-174.CrossRefPubMed Faupel-Badger JM, Arcaro KF, Balkam JJ, Eliassen AH, Hassiotou F, Lebrilla CB, Michels KB, Palmer JR, Schedin P, Stuebe AM, Watson CJ, Sherman ME: Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute–sponsored workshop. J Natl Cancer Inst. 2013, 105: 166-174.CrossRefPubMed
11.
go back to reference Layde PM, Webster LA, Baughman AL, Wingo PA, Rubin GL, Ory HW: The independent associations of parity, age at first full term pregnancy, and duration of breastfeeding with the risk of breast cancer. J Clin Epidemiol. 1989, 42: 963-973.CrossRefPubMed Layde PM, Webster LA, Baughman AL, Wingo PA, Rubin GL, Ory HW: The independent associations of parity, age at first full term pregnancy, and duration of breastfeeding with the risk of breast cancer. J Clin Epidemiol. 1989, 42: 963-973.CrossRefPubMed
12.
go back to reference Belitskaya-Lévy I, Zeleniuch-Jacquotte A, Russo J, Russo IH, Bordás P, Ahman J, Afanasyeva Y, Johansson R, Lenner P, Li X, de Cicco RL, Peri S, Ross E, Russo PA, Santucci-Pereira J, Sheriff FS, Slifker M, Hallmans G, Toniolo P, Arslan AA: Characterization of a genomic signature of pregnancy identified in the breast. Cancer Prev Res (Phila). 2011, 4: 1457-1464.CrossRef Belitskaya-Lévy I, Zeleniuch-Jacquotte A, Russo J, Russo IH, Bordás P, Ahman J, Afanasyeva Y, Johansson R, Lenner P, Li X, de Cicco RL, Peri S, Ross E, Russo PA, Santucci-Pereira J, Sheriff FS, Slifker M, Hallmans G, Toniolo P, Arslan AA: Characterization of a genomic signature of pregnancy identified in the breast. Cancer Prev Res (Phila). 2011, 4: 1457-1464.CrossRef
13.
go back to reference Russo J, Santucci-Pereira J, de Cicco RL, Sheriff F, Russo PA, Peri S, Slifker M, Ross E, Mello ML, Vidal BC, Belitskaya-Lévy I, Arslan A, Zeleniuch-Jacquotte A, Bordas P, Lenner P, Ahman J, Afanasyeva Y, Hallmans G, Toniolo P, Russo IH: Pregnancy-induced chromatin remodeling in the breast of postmenopausal women. Int J Cancer. 2012, 131: 1059-1070.CrossRefPubMedPubMedCentral Russo J, Santucci-Pereira J, de Cicco RL, Sheriff F, Russo PA, Peri S, Slifker M, Ross E, Mello ML, Vidal BC, Belitskaya-Lévy I, Arslan A, Zeleniuch-Jacquotte A, Bordas P, Lenner P, Ahman J, Afanasyeva Y, Hallmans G, Toniolo P, Russo IH: Pregnancy-induced chromatin remodeling in the breast of postmenopausal women. Int J Cancer. 2012, 131: 1059-1070.CrossRefPubMedPubMedCentral
14.
go back to reference Peri S, de Cicco RL, Santucci-Pereira J, Slifker M, Ross EA, Russo IH, Russo PA, Arslan AA, Belitskaya-Lévy I, Zeleniuch-Jacquotte A, Bordas P, Lenner P, Åhman J, Afanasyeva Y, Johansson R, Sheriff F, Hallmans G, Toniolo P, Russo J: Defining the genomic signature of the parous breast. BMC Med Genomics. 2012, 5: 46-CrossRefPubMedPubMedCentral Peri S, de Cicco RL, Santucci-Pereira J, Slifker M, Ross EA, Russo IH, Russo PA, Arslan AA, Belitskaya-Lévy I, Zeleniuch-Jacquotte A, Bordas P, Lenner P, Åhman J, Afanasyeva Y, Johansson R, Sheriff F, Hallmans G, Toniolo P, Russo J: Defining the genomic signature of the parous breast. BMC Med Genomics. 2012, 5: 46-CrossRefPubMedPubMedCentral
15.
go back to reference Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC: Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006, 295: 2492-2502.CrossRefPubMed Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC: Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006, 295: 2492-2502.CrossRefPubMed
16.
go back to reference Perou CM, Parker JS, Prat A, Ellis MJ, Bernard PS: Clinical implementation of the intrinsic subtypes of breast cancer. Lancet Oncol. 2010, 11: 718-721.CrossRefPubMed Perou CM, Parker JS, Prat A, Ellis MJ, Bernard PS: Clinical implementation of the intrinsic subtypes of breast cancer. Lancet Oncol. 2010, 11: 718-721.CrossRefPubMed
17.
go back to reference Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lønning PE, Børresen-Dale AL: Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001, 98: 10869-10874.CrossRefPubMedPubMedCentral Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lønning PE, Børresen-Dale AL: Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001, 98: 10869-10874.CrossRefPubMedPubMedCentral
18.
go back to reference Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B, Hewitt SM, Anderson WF, Szeszenia-Dabrowska N, Bardin-Mikolajczak A, Zatonski W, Cartun R, Mandich D, Rymkiewicz G, Ligaj M, Lukaszek S, Kordek R, García-Closas M: Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev. 2007, 16: 439-443.CrossRefPubMed Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B, Hewitt SM, Anderson WF, Szeszenia-Dabrowska N, Bardin-Mikolajczak A, Zatonski W, Cartun R, Mandich D, Rymkiewicz G, Ligaj M, Lukaszek S, Kordek R, García-Closas M: Differences in risk factors for breast cancer molecular subtypes in a population-based study. Cancer Epidemiol Biomarkers Prev. 2007, 16: 439-443.CrossRefPubMed
19.
go back to reference Shinde SS, Forman MR, Kuerer HM, Yan K, Peintinger F, Hunt KK, Hortobagyi GN, Pusztai L, Symmans WF: Higher parity and shorter breastfeeding duration: association with triple-negative phenotype of breast cancer. Cancer. 2010, 116: 4933-4943.CrossRefPubMed Shinde SS, Forman MR, Kuerer HM, Yan K, Peintinger F, Hunt KK, Hortobagyi GN, Pusztai L, Symmans WF: Higher parity and shorter breastfeeding duration: association with triple-negative phenotype of breast cancer. Cancer. 2010, 116: 4933-4943.CrossRefPubMed
20.
go back to reference Li CI, Beaber EF, Tang MT, Porter PL, Daling JR, Malone KE: Reproductive factors and risk of estrogen receptor positive, triple-negative, and HER2-neu overexpressing breast cancer among women 20–44 years of age. Breast Cancer Res Treat. 2013, 137: 579-587.CrossRefPubMed Li CI, Beaber EF, Tang MT, Porter PL, Daling JR, Malone KE: Reproductive factors and risk of estrogen receptor positive, triple-negative, and HER2-neu overexpressing breast cancer among women 20–44 years of age. Breast Cancer Res Treat. 2013, 137: 579-587.CrossRefPubMed
21.
go back to reference Gaudet MM, Press MF, Haile RW, Lynch CF, Glaser SL, Schildkraut J, Gammon MD, Douglas Thompson W, Bernstein JL: Risk factors by molecular subtypes of breast cancer across a population-based study of women 56 years or younger. Breast Cancer Res Treat. 2011, 130: 587-597.CrossRefPubMedPubMedCentral Gaudet MM, Press MF, Haile RW, Lynch CF, Glaser SL, Schildkraut J, Gammon MD, Douglas Thompson W, Bernstein JL: Risk factors by molecular subtypes of breast cancer across a population-based study of women 56 years or younger. Breast Cancer Res Treat. 2011, 130: 587-597.CrossRefPubMedPubMedCentral
22.
go back to reference Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, Smith LV, Labbok MH, Geradts J, Bensen JT, Jackson S, Nyante S, Livasy C, Carey L, Earp HS, Perou CM: Epidemiology of basal-like breast cancer. Breast Cancer Res Treat. 2008, 109: 123-139.CrossRefPubMed Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, Smith LV, Labbok MH, Geradts J, Bensen JT, Jackson S, Nyante S, Livasy C, Carey L, Earp HS, Perou CM: Epidemiology of basal-like breast cancer. Breast Cancer Res Treat. 2008, 109: 123-139.CrossRefPubMed
23.
go back to reference Palmer JR, Boggs DA, Wise LA, Ambrosone CB, Adams-Campbell LL, Rosenberg L: Parity and lactation in relation to estrogen receptor negative breast cancer in African American women. Cancer Epidemiol Biomarkers Prev. 2011, 20: 1883-1891.CrossRefPubMedPubMedCentral Palmer JR, Boggs DA, Wise LA, Ambrosone CB, Adams-Campbell LL, Rosenberg L: Parity and lactation in relation to estrogen receptor negative breast cancer in African American women. Cancer Epidemiol Biomarkers Prev. 2011, 20: 1883-1891.CrossRefPubMedPubMedCentral
24.
go back to reference Asztalos S, Gann PH, Hayes MK, Nonn L, Beam CA, Dai Y, Wiley EL, Tonetti DA: Gene expression patterns in the human breast after pregnancy. Cancer Prev Res (Phila). 2010, 3: 301-311.CrossRef Asztalos S, Gann PH, Hayes MK, Nonn L, Beam CA, Dai Y, Wiley EL, Tonetti DA: Gene expression patterns in the human breast after pregnancy. Cancer Prev Res (Phila). 2010, 3: 301-311.CrossRef
25.
go back to reference García-Closas M, Brinton LA, Lissowska J, Chatterjee N, Peplonska B, Anderson WF, Szeszenia-Dabrowska N, Bardin-Mikolajczak A, Zatonski W, Blair A, Kalaylioglu Z, Rymkiewicz G, Mazepa-Sikora D, Kordek R, Lukaszek S, Sherman ME: Established breast cancer risk factors by clinically important tumour characteristics. Br J Cancer. 2006, 95: 123-129.CrossRefPubMedPubMedCentral García-Closas M, Brinton LA, Lissowska J, Chatterjee N, Peplonska B, Anderson WF, Szeszenia-Dabrowska N, Bardin-Mikolajczak A, Zatonski W, Blair A, Kalaylioglu Z, Rymkiewicz G, Mazepa-Sikora D, Kordek R, Lukaszek S, Sherman ME: Established breast cancer risk factors by clinically important tumour characteristics. Br J Cancer. 2006, 95: 123-129.CrossRefPubMedPubMedCentral
26.
go back to reference Sun X, Casbas-Hernandez P, Bigelow C, Makowski L, Jerry DJ, Smith Schneider S, Troester MA: Normal breast tissue of obese women is enriched for macrophage markers and macrophage-associated gene expression. Breast Cancer Res Treat. 2012, 131: 1003-1012.CrossRefPubMed Sun X, Casbas-Hernandez P, Bigelow C, Makowski L, Jerry DJ, Smith Schneider S, Troester MA: Normal breast tissue of obese women is enriched for macrophage markers and macrophage-associated gene expression. Breast Cancer Res Treat. 2012, 131: 1003-1012.CrossRefPubMed
27.
go back to reference Troester MA, Lee MH, Carter M, Fan C, Cowan DW, Perez ER, Pirone JR, Perou CM, Jerry DJ, Schneider SS: Activation of host wound responses in breast cancer microenvironment. Clin Cancer Res. 2009, 15: 7020-7028.CrossRefPubMedPubMedCentral Troester MA, Lee MH, Carter M, Fan C, Cowan DW, Perez ER, Pirone JR, Perou CM, Jerry DJ, Schneider SS: Activation of host wound responses in breast cancer microenvironment. Clin Cancer Res. 2009, 15: 7020-7028.CrossRefPubMedPubMedCentral
28.
go back to reference Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001, 98: 5116-5121. A published erratum appears in Proc Natl Acad Sci U S A 2001, 98:10515CrossRefPubMedPubMedCentral Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001, 98: 5116-5121. A published erratum appears in Proc Natl Acad Sci U S A 2001, 98:10515CrossRefPubMedPubMedCentral
29.
go back to reference Page RD: Visualizing phylogenetic trees using TreeView. Curr Protoc Bioinformatics. 2002, Chapter 6: Unit 6.2-PubMed Page RD: Visualizing phylogenetic trees using TreeView. Curr Protoc Bioinformatics. 2002, Chapter 6: Unit 6.2-PubMed
30.
go back to reference Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN: GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 2003, 4: R28-CrossRefPubMedPubMedCentral Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN: GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 2003, 4: R28-CrossRefPubMedPubMedCentral
31.
go back to reference Camp JT, Elloumi F, Roman-Perez E, Rein J, Stewart DA, Harrell JC, Perou CM, Troester MA: Interactions with fibroblasts are distinct in basal-like and luminal breast cancers. Mol Cancer Res. 2011, 9: 3-13.CrossRefPubMed Camp JT, Elloumi F, Roman-Perez E, Rein J, Stewart DA, Harrell JC, Perou CM, Troester MA: Interactions with fibroblasts are distinct in basal-like and luminal breast cancers. Mol Cancer Res. 2011, 9: 3-13.CrossRefPubMed
32.
go back to reference Yang XR, Pfeiffer RM, Garcia-Closas M, Rimm DL, Lissowska J, Brinton LA, Peplonska B, Hewitt SM, Cartun RW, Mandich D, Sasano H, Evans DB, Sutter TR, Sherman ME: Hormonal markers in breast cancer: coexpression, relationship with pathologic characteristics, and risk factor associations in a population-based study. Cancer Res. 2007, 67: 10608-10617.CrossRefPubMed Yang XR, Pfeiffer RM, Garcia-Closas M, Rimm DL, Lissowska J, Brinton LA, Peplonska B, Hewitt SM, Cartun RW, Mandich D, Sasano H, Evans DB, Sutter TR, Sherman ME: Hormonal markers in breast cancer: coexpression, relationship with pathologic characteristics, and risk factor associations in a population-based study. Cancer Res. 2007, 67: 10608-10617.CrossRefPubMed
33.
go back to reference Sherman ME, Rimm DL, Yang XR, Chatterjee N, Brinton LA, Lissowska J, Peplonska B, Szeszenia-Dabrowska N, Zatonski W, Cartun R, Mandich D, Rymkiewicz G, Ligaj M, Lukaszek S, Kordek R, Kalaylioglu Z, Harigopal M, Charrette L, Falk RT, Richesson D, Anderson WF, Hewitt SM, García-Closas M: Variation in breast cancer hormone receptor and HER2 levels by etiologic factors: A population-based analysis. Int J Cancer. 2007, 121: 1079-1085.CrossRefPubMed Sherman ME, Rimm DL, Yang XR, Chatterjee N, Brinton LA, Lissowska J, Peplonska B, Szeszenia-Dabrowska N, Zatonski W, Cartun R, Mandich D, Rymkiewicz G, Ligaj M, Lukaszek S, Kordek R, Kalaylioglu Z, Harigopal M, Charrette L, Falk RT, Richesson D, Anderson WF, Hewitt SM, García-Closas M: Variation in breast cancer hormone receptor and HER2 levels by etiologic factors: A population-based analysis. Int J Cancer. 2007, 121: 1079-1085.CrossRefPubMed
34.
go back to reference Sun X, Gierach GL, Sandhu R, Williams T, Midkiff BR, Lissowska J, Wesolowska E, Boyd NF, Johnson NB, Figueroa JD, Sherman ME, Troester MA: Relationship of mammographic density and gene expression: analysis of normal breast tissue surrounding breast cancer. Clin Cancer Res. 2013, 19: 4972-4982.CrossRefPubMedPubMedCentral Sun X, Gierach GL, Sandhu R, Williams T, Midkiff BR, Lissowska J, Wesolowska E, Boyd NF, Johnson NB, Figueroa JD, Sherman ME, Troester MA: Relationship of mammographic density and gene expression: analysis of normal breast tissue surrounding breast cancer. Clin Cancer Res. 2013, 19: 4972-4982.CrossRefPubMedPubMedCentral
35.
go back to reference Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP: Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005, 102: 15545-15550.CrossRefPubMedPubMedCentral Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP: Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005, 102: 15545-15550.CrossRefPubMedPubMedCentral
36.
go back to reference Creighton CJ, Casa A, Lazard Z, Huang S, Tsimelzon A, Hilsenbeck SG, Osborne CK, Lee AV: Insulin-like growth factor-I activates gene transcription programs strongly associated with poor breast cancer prognosis. J Clin Oncol. 2008, 26: 4078-4085.CrossRefPubMedPubMedCentral Creighton CJ, Casa A, Lazard Z, Huang S, Tsimelzon A, Hilsenbeck SG, Osborne CK, Lee AV: Insulin-like growth factor-I activates gene transcription programs strongly associated with poor breast cancer prognosis. J Clin Oncol. 2008, 26: 4078-4085.CrossRefPubMedPubMedCentral
38.
go back to reference Stein T, Morris JS, Davies CR, Weber-Hall SJ, Duffy MA, Heath VJ, Bell AK, Ferrier RK, Sandilands GP, Gusterson BA: Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Res. 2004, 6: R75-R91.CrossRefPubMed Stein T, Morris JS, Davies CR, Weber-Hall SJ, Duffy MA, Heath VJ, Bell AK, Ferrier RK, Sandilands GP, Gusterson BA: Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3. Breast Cancer Res. 2004, 6: R75-R91.CrossRefPubMed
39.
go back to reference Clarkson RW, Wayland MT, Lee J, Freeman T, Watson CJ: Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Res. 2004, 6: R92-R109.CrossRefPubMed Clarkson RW, Wayland MT, Lee J, Freeman T, Watson CJ: Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression. Breast Cancer Res. 2004, 6: R92-R109.CrossRefPubMed
40.
go back to reference D’Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, Cox JD, Wang JY, Ha SI, Keister BA, Chodosh LA: Persistent parity-induced changes in growth factors, TGF-β3, and differentiation in the rodent mammary gland. Mol Endocrinol. 2002, 16: 2034-2051.CrossRefPubMed D’Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, Cox JD, Wang JY, Ha SI, Keister BA, Chodosh LA: Persistent parity-induced changes in growth factors, TGF-β3, and differentiation in the rodent mammary gland. Mol Endocrinol. 2002, 16: 2034-2051.CrossRefPubMed
41.
go back to reference Csanaky K, Doppler W, Tamas A, Kovacs K, Toth G, Reglodi DJ: Influence of terminal differentiation and PACAP on the cytokine, chemokine, and growth factor secretion of mammary epithelial cells. Mol Neurosci. 2014, 52: 28-36.CrossRef Csanaky K, Doppler W, Tamas A, Kovacs K, Toth G, Reglodi DJ: Influence of terminal differentiation and PACAP on the cytokine, chemokine, and growth factor secretion of mammary epithelial cells. Mol Neurosci. 2014, 52: 28-36.CrossRef
42.
go back to reference Meier-Abt F, Milani E, Roloff T, Brinkhaus H, Duss S, Meyer DS, Klebba I, Balwierz PJ, van Nimwegen E, Bentires-Alj M: Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium. Breast Cancer Res. 2013, 15: R36-CrossRefPubMedPubMedCentral Meier-Abt F, Milani E, Roloff T, Brinkhaus H, Duss S, Meyer DS, Klebba I, Balwierz PJ, van Nimwegen E, Bentires-Alj M: Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium. Breast Cancer Res. 2013, 15: R36-CrossRefPubMedPubMedCentral
43.
go back to reference Finak G, Sadekova S, Pepin F, Hallett M, Meterissian S, Halwani F, Khetani K, Souleimanova M, Zabolotny B, Omeroglu A, Park M: Gene expression signatures of morphologically normal breast tissue identify basal-like tumors. Breast Cancer Res. 2006, 8: R58-CrossRefPubMedPubMedCentral Finak G, Sadekova S, Pepin F, Hallett M, Meterissian S, Halwani F, Khetani K, Souleimanova M, Zabolotny B, Omeroglu A, Park M: Gene expression signatures of morphologically normal breast tissue identify basal-like tumors. Breast Cancer Res. 2006, 8: R58-CrossRefPubMedPubMedCentral
45.
go back to reference Merlo LM, Pepper JW, Reid BJ, Maley CC: Cancer as an evolutionary and ecological process. Nat Rev Cancer. 2006, 6: 924-935.CrossRefPubMed Merlo LM, Pepper JW, Reid BJ, Maley CC: Cancer as an evolutionary and ecological process. Nat Rev Cancer. 2006, 6: 924-935.CrossRefPubMed
46.
go back to reference Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, Schnitt S, Sellers WR, Polyak K: Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004, 6: 17-32.CrossRefPubMed Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, Schnitt S, Sellers WR, Polyak K: Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004, 6: 17-32.CrossRefPubMed
47.
go back to reference Bissell MJ, Hines WC: Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med. 2011, 17: 320-329.CrossRefPubMedPubMedCentral Bissell MJ, Hines WC: Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med. 2011, 17: 320-329.CrossRefPubMedPubMedCentral
48.
go back to reference Hartman J, Ström A, Gustafsson JÅ: Estrogen receptor β in breast cancer—diagnostic and therapeutic implications. Steroids. 2009, 74: 635-641.CrossRefPubMed Hartman J, Ström A, Gustafsson JÅ: Estrogen receptor β in breast cancer—diagnostic and therapeutic implications. Steroids. 2009, 74: 635-641.CrossRefPubMed
49.
50.
go back to reference Robinson WR, Cheng MC, Hoggatt KJ, Stürmer T, Siega-Riz AM: Childbearing is not associated with young women’s long-term obesity risk. Obesity (Silver Spring). 2014, 22: 1126-1132.CrossRef Robinson WR, Cheng MC, Hoggatt KJ, Stürmer T, Siega-Riz AM: Childbearing is not associated with young women’s long-term obesity risk. Obesity (Silver Spring). 2014, 22: 1126-1132.CrossRef
51.
go back to reference Wells JC, Griffin L, Treleaven P: Independent changes in female body shape with parity and age: A life-history approach to female adiposity. Am J Hum Biol. 2010, 22: 456-462.CrossRefPubMed Wells JC, Griffin L, Treleaven P: Independent changes in female body shape with parity and age: A life-history approach to female adiposity. Am J Hum Biol. 2010, 22: 456-462.CrossRefPubMed
52.
go back to reference Pirone JR, D’Arcy M, Stewart DA, Hines WC, Johnson M, Gould MN, Yaswen P, Jerry DJ, Smith Schneider S, Troester MA: Age-associated gene expression in normal breast tissue mirrors qualitative age-at-incidence patterns for breast cancer. Cancer Epidemiol Biomarkers Prev. 2012, 21: 1735-1744.CrossRefPubMedPubMedCentral Pirone JR, D’Arcy M, Stewart DA, Hines WC, Johnson M, Gould MN, Yaswen P, Jerry DJ, Smith Schneider S, Troester MA: Age-associated gene expression in normal breast tissue mirrors qualitative age-at-incidence patterns for breast cancer. Cancer Epidemiol Biomarkers Prev. 2012, 21: 1735-1744.CrossRefPubMedPubMedCentral
Metadata
Title
Parity-related molecular signatures and breast cancer subtypes by estrogen receptor status
Authors
Melissa Rotunno
Xuezheng Sun
Jonine Figueroa
Mark E Sherman
Montserrat Garcia-Closas
Paul Meltzer
Tyisha Williams
Sallie Smith Schneider
D Joseph Jerry
Xiaohong R Yang
Melissa A Troester
Publication date
01-02-2014
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2014
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/bcr3689

Other articles of this Issue 1/2014

Breast Cancer Research 1/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine