An interferon signature identified by RNA-sequencing of mammary tissues varies across the estrous cycle and is predictive of metastasis-free survival
Abstract
The concept that a breast cancer patient's menstrual stage at the time of tumor surgery influences risk of metastases remains controversial. The scarcity of comprehensive molecular studies of menstrual stage-dependent fluctuations in the breast provides little insight. To gain a deeper understanding of the biological changes in mammary tissue and blood during the menstrual cycle and to determine the influence of environmental exposures, such as low-dose ionizing radiation (LDIR), we used the mouse to characterize estrous-cycle variations in mammary gene transcripts by RNA-sequencing, peripheral white blood cell (WBC) counts and plasma cytokine levels. We identified an estrous-variable and hormone-dependent gene cluster enriched for Type-1 interferon genes. Cox regression identified a 117-gene signature of interferon-associated genes, which correlated with lower frequencies of metastasis in breast cancer patients. LDIR (10cGy) exposure had no detectable effect on mammary transcripts. However, peripheral WBC counts varied across the estrous cycle and LDIR exposure reduced lymphocyte counts and cytokine levels in tumor-susceptible mice. Our finding of variations in mammary Type-1 interferon and immune functions across the estrous cycle provides a mechanism by which timing of breast tumor surgery during the menstrual cycle may have clinical relevance to a patient's risk for distant metastases.
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1407216
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Oncotarget
- Additional Journal Information:
- Journal Volume: 5; Journal Issue: 12; Journal ID: ISSN 1949-2553
- Publisher:
- Impact Journals
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; estrous cycle; mammary glad; RNA-sequencing; Type-1 interferon; low-dose radiation (LDIR); immunity; breast cancer; genetic susceptibility
Citation Formats
Snijders, Antoine M., Langley, Sasha, Mao, Jian-Hua, Bhatnagar, Sandhya, Bjornstad, Kathleen A., Rosen, Chris J., Lo, Alvin, Huang, Yurong, Blakely, Eleanor A., Karpen, Gary H., Bissell, Mina J., and Wyrobek, Andrew J. An interferon signature identified by RNA-sequencing of mammary tissues varies across the estrous cycle and is predictive of metastasis-free survival. United States: N. p., 2014.
Web. doi:10.18632/oncotarget.2148.
Snijders, Antoine M., Langley, Sasha, Mao, Jian-Hua, Bhatnagar, Sandhya, Bjornstad, Kathleen A., Rosen, Chris J., Lo, Alvin, Huang, Yurong, Blakely, Eleanor A., Karpen, Gary H., Bissell, Mina J., & Wyrobek, Andrew J. An interferon signature identified by RNA-sequencing of mammary tissues varies across the estrous cycle and is predictive of metastasis-free survival. United States. https://doi.org/10.18632/oncotarget.2148
Snijders, Antoine M., Langley, Sasha, Mao, Jian-Hua, Bhatnagar, Sandhya, Bjornstad, Kathleen A., Rosen, Chris J., Lo, Alvin, Huang, Yurong, Blakely, Eleanor A., Karpen, Gary H., Bissell, Mina J., and Wyrobek, Andrew J. Mon .
"An interferon signature identified by RNA-sequencing of mammary tissues varies across the estrous cycle and is predictive of metastasis-free survival". United States. https://doi.org/10.18632/oncotarget.2148. https://www.osti.gov/servlets/purl/1407216.
@article{osti_1407216,
title = {An interferon signature identified by RNA-sequencing of mammary tissues varies across the estrous cycle and is predictive of metastasis-free survival},
author = {Snijders, Antoine M. and Langley, Sasha and Mao, Jian-Hua and Bhatnagar, Sandhya and Bjornstad, Kathleen A. and Rosen, Chris J. and Lo, Alvin and Huang, Yurong and Blakely, Eleanor A. and Karpen, Gary H. and Bissell, Mina J. and Wyrobek, Andrew J.},
abstractNote = {The concept that a breast cancer patient's menstrual stage at the time of tumor surgery influences risk of metastases remains controversial. The scarcity of comprehensive molecular studies of menstrual stage-dependent fluctuations in the breast provides little insight. To gain a deeper understanding of the biological changes in mammary tissue and blood during the menstrual cycle and to determine the influence of environmental exposures, such as low-dose ionizing radiation (LDIR), we used the mouse to characterize estrous-cycle variations in mammary gene transcripts by RNA-sequencing, peripheral white blood cell (WBC) counts and plasma cytokine levels. We identified an estrous-variable and hormone-dependent gene cluster enriched for Type-1 interferon genes. Cox regression identified a 117-gene signature of interferon-associated genes, which correlated with lower frequencies of metastasis in breast cancer patients. LDIR (10cGy) exposure had no detectable effect on mammary transcripts. However, peripheral WBC counts varied across the estrous cycle and LDIR exposure reduced lymphocyte counts and cytokine levels in tumor-susceptible mice. Our finding of variations in mammary Type-1 interferon and immune functions across the estrous cycle provides a mechanism by which timing of breast tumor surgery during the menstrual cycle may have clinical relevance to a patient's risk for distant metastases.},
doi = {10.18632/oncotarget.2148},
journal = {Oncotarget},
number = 12,
volume = 5,
place = {United States},
year = {Mon Jun 30 00:00:00 EDT 2014},
month = {Mon Jun 30 00:00:00 EDT 2014}
}
Web of Science
Works referenced in this record:
Finding consistent patterns: A nonparametric approach for identifying differential expression in RNA-Seq data
journal, November 2011
- Li, Jun; Tibshirani, Robert
- Statistical Methods in Medical Research, Vol. 22, Issue 5
Serum progesterone and prognosis in operable breast cancer
journal, June 1996
- Mohr, Pe; Wang, Dy; Gregory, Wm
- British Journal of Cancer, Vol. 73, Issue 12
Dual roles for macrophages in ovarian cycle-associated development and remodelling of the mammary gland epithelium
journal, December 2010
- Chua, Angela C. L.; Hodson, Leigh J.; Moldenhauer, Lachlan M.
- Development, Vol. 137, Issue 24
TNFα acting on TNFR1 promotes breast cancer growth via p42/P44 MAPK, JNK, Akt and NF-κB-dependent pathways
journal, February 2008
- Rivas, Martín A.; Carnevale, Romina P.; Proietti, Cecilia J.
- Experimental Cell Research, Vol. 314, Issue 3
Low doses of ionizing radiation induce immune-stimulatory responses in isolated human primary monocytes
journal, September 2013
- El-Saghire, Houssein; Michaux, Arlette; Thierens, Hubert
- International Journal of Molecular Medicine, Vol. 32, Issue 6
RESPONSE Re: The Influence of Menstrual Cycle Phase on Surgical Treatment of Primary Breast Cancer: Have We Made Any Progress Over the Past 13 Years?
journal, November 2002
- Hortobagyi, G.
- CancerSpectrum Knowledge Environment, Vol. 94, Issue 22
The Relationship between Surgery and Phase of the Menstrual Cycle Affects Survival in Breast Cancer
journal, January 2012
- Kucuk, Ali Imran; Atalay, Can
- Journal of Breast Cancer, Vol. 15, Issue 4
Metabolic regulation in the lactating mammary gland: a lipid synthesizing machine
journal, February 2007
- Rudolph, Michael C.; McManaman, James L.; Phang, TzuLip
- Physiological Genomics, Vol. 28, Issue 3
Antitumor effects of interleukin-12 in pre-clinical and early clinical studies (Review).
journal, May 1999
- Golab, J.; Zagozdzon, R.
- International Journal of Molecular Medicine
Cancer in the Contralateral Breast after Radiotherapy for Breast Cancer
journal, March 1992
- Boice, John D.; Harvey, Elizabeth B.; Blettner, Maria
- New England Journal of Medicine, Vol. 326, Issue 12
Timing of breast cancer surgery: nodes, hormones, and retrospectoscopy
journal, June 1994
- Astrow, AlanB.
- The Lancet, Vol. 343, Issue 8912
Comparison of Four Nuclear Isolation Buffers for Plant DNA Flow Cytometry
journal, July 2006
- Loureiro, JoÃO; Rodriguez, Eleazar; DoleŽEl, Jaroslav
- Annals of Botany, Vol. 98, Issue 3
Serum progesterone at the time of surgery and survival in women with premenopausal operable breast cancer
journal, January 1994
- Badwe, R. A.; Wang, D. Y.; Gregory, W. M.
- European Journal of Cancer, Vol. 30, Issue 4
Changes in the levels of superoxide anion radical and superoxide dismutase during the estrous cycle of Rattusnorvegicus and induction of superoxide dismutase in rat ovary by lutropin
journal, November 1988
- Laloraya, Malini; Pradeep kumar, G.; Laloraya, Manmohan M.
- Biochemical and Biophysical Research Communications, Vol. 157, Issue 1
Regulation of type I interferon responses
journal, December 2013
- Ivashkiv, Lionel B.; Donlin, Laura T.
- Nature Reviews Immunology, Vol. 14, Issue 1
Timing of breast cancer surgery in relation to menstrual cycle phase: no effect on 3-year prognosis: The ITS Study
journal, December 2007
- Thorpe, H.; Brown, S. R.; Sainsbury, J. R.
- British Journal of Cancer, Vol. 98, Issue 1
Interferon-ε Protects the Female Reproductive Tract from Viral and Bacterial Infection
journal, March 2013
- Fung, Ka Yee; Mangan, Niamh E.; Cumming, Helen
- Science, Vol. 339, Issue 6123
Influence of the estrous cycle at gamma-ray exposure on radiation-induced mammary tumorigenesis in virgin rats
journal, September 1992
- Inano, Hiroshi; Ishii-Ohba, Hiroko; Suzuki, Keiko
- International Journal of Cancer, Vol. 52, Issue 3
Differential expression analysis for sequence count data
journal, April 2010
- Anders, Simon; Huber, Wolfgang
- Nature Precedings
Timing of Breast Cancer Excision during the Menstrual Cycle Influences Duration of Disease-free Survival
journal, September 1991
- Senie, Ruby T.; Rosen, Paul Peter; Rhodes, Philip
- Annals of Internal Medicine, Vol. 115, Issue 5
The A and B Isoforms of the Human Progesterone Receptor Operate through Distinct Signaling Pathways within Target Cells
journal, December 1994
- Wen, Dawn X.; Xu, You-Feng; Mais, Dale E.
- Molecular and Cellular Biology, Vol. 14, Issue 12
Next-generation transcriptome sequencing of the premenopausal breast epithelium using specimens from a normal human breast tissue bank
journal, March 2014
- Pardo, Ivanesa; Lillemoe, Heather A.; Blosser, Rachel J.
- Breast Cancer Research, Vol. 16, Issue 2
INTERFEROME v2.0: an updated database of annotated interferon-regulated genes
journal, November 2012
- Rusinova, Irina; Forster, Sam; Yu, Simon
- Nucleic Acids Research, Vol. 41, Issue D1
Estrous influence on surgical cure of a mouse breast cancer.
journal, July 1988
- Ratajczak, H. V.; Sothern, R. B.; Hrushesky, W. J.
- Journal of Experimental Medicine, Vol. 168, Issue 1
IRF-7 is the master regulator of type-I interferon-dependent immune responses
journal, March 2005
- Honda, Kenya; Yanai, Hideyuki; Negishi, Hideo
- Nature, Vol. 434, Issue 7034
Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression
journal, September 2009
- Fujimoto, Hiroshi; Sangai, Takafumi; Ishii, Genichiro
- International Journal of Cancer, Vol. 125, Issue 6
The Emerging Role of Immunosurveillance in Dictating Metastatic Spread in Breast Cancer
journal, October 2013
- Slaney, Clare Y.; Rautela, Jai; Parker, Belinda S.
- Cancer Research, Vol. 73, Issue 19
Biodosimetry Medical Recording—Use of the Biodosimetry Assessment Tool
journal, November 2010
- Blakely, William F.; Madrid, John P.; Sandgren, David J.
- Health Physics, Vol. 99, Issue 5
Different Regions of the Estrogen Receptor Are Required for Synergistic Action with the Glucocorticoid and Progesterone Receptors
journal, December 1989
- Cato, Andrew C. B.; Ponta, Helmut
- Molecular and Cellular Biology, Vol. 9, Issue 12
Study of antioxidative effects and anti-inflammatory effects in mice due to low-dose X-irradiation or radon inhalation
journal, February 2013
- Kataoka, T.
- Journal of Radiation Research, Vol. 54, Issue 4
Menstrual Cycle and Surgical Treatment of Breast Cancer: Findings From the NCCTG N9431 Study
journal, August 2009
- Grant, Clive S.; Ingle, James N.; Suman, Vera J.
- Journal of Clinical Oncology, Vol. 27, Issue 22
HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014
- Anders, S.; Pyl, P. T.; Huber, W.
- Bioinformatics, Vol. 31, Issue 2
Timing of Surgery During Menstrual Cycle and Survival of Premenopausal Women With Operable Breast Cancer
journal, February 1992
- Badwe, R. A.; Gregory, W. M.; Chaudary, M. A.
- Obstetrical & Gynecological Survey, Vol. 47, Issue 2
Candidate Genes Associated with Tumor Regression Mediated by Intratumoral Il-12 Electroporation Gene Therapy
journal, March 2004
- Li, Shulin; Xia, Xueqing; Mellieon, Francesca M.
- Molecular Therapy, Vol. 9, Issue 3
Menstrual influence on surgical cure of breast cancer
journal, April 1990
- Hrushesky, WilliamJ. M.; Bluming, AvrumZ.; Gruber, ScottA.
- The Lancet, Vol. 335, Issue 8695
Adaptive immunity maintains occult cancer in an equilibrium state
journal, November 2007
- Koebel, Catherine M.; Vermi, William; Swann, Jeremy B.
- Nature, Vol. 450, Issue 7171
Eotaxin Is Required for Eosinophil Homing into the Stroma of the Pubertal and Cycling Uterus
journal, October 2001
- Gouon-Evans, Valérie; Pollard, Jeffrey W.
- Endocrinology, Vol. 142, Issue 10
Menstrual Cycle Timing of Breast Cancer Resection: Prospective Study Is Overdue
journal, January 1995
- Hrushesky, W. J. M.
- JNCI Journal of the National Cancer Institute, Vol. 87, Issue 2
Lymphocyte Counts Independently Predict Overall Survival in Advanced Cancer Patients: A Biomarker for IL-2 Immunotherapy
journal, September 2003
- Fumagalli, Luca A.; Vinke, Jan; Hoff, Wilco
- Journal of Immunotherapy, Vol. 26, Issue 5
The Influence of Menstrual Cycle Phase on Surgical Treatment of Primary Breast Cancer: Have We Made Any Progress Over the Past 13 Years?
journal, May 2002
- Hortobagyi, G. N.
- CancerSpectrum Knowledge Environment, Vol. 94, Issue 9
Does the Timing of Breast Cancer Surgery Affect Survival?
journal, April 1997
- Randal, J.
- JNCI Journal of the National Cancer Institute, Vol. 89, Issue 7
Menstrual Cycle Timing of Breast Cancer Resection: Prospective Study Is Overdue
journal, January 1995
- Hrushesky, W. J. M.
- JNCI Journal of the National Cancer Institute, Vol. 87, Issue 2
Optimal Timing of Breast Cancer Surgery: Findings Revive Debate
journal, April 1993
- Larsen, N. S.
- JNCI Journal of the National Cancer Institute, Vol. 85, Issue 8
Timing of Breast Cancer Excision during the Menstrual Cycle Influences Duration of Disease-free Survival
journal, September 1991
- Senie, Ruby T.; Rosen, Paul Peter; Rhodes, Philip
- Annals of Internal Medicine, Vol. 115, Issue 5
Timing of surgery during menstrual cycle and survival of premenopausal women with operable breast cancer
journal, May 1991
- Badwe, R. A.; Gregory, W. M.; Chaudary, M. A.
- The Lancet, Vol. 337, Issue 8752
The Relationship between Surgery and Phase of the Menstrual Cycle Affects Survival in Breast Cancer
journal, January 2012
- Kucuk, Ali Imran; Atalay, Can
- Journal of Breast Cancer, Vol. 15, Issue 4
Effect of menstrual phase on surgical treatment of breast cancer
journal, June 1994
- Veronesi, U.; Luini, A.; Mariani, L.
- The Lancet, Vol. 343, Issue 8912
Serum progesterone and prognosis in operable breast cancer
journal, June 1996
- Mohr, Pe; Wang, Dy; Gregory, Wm
- British Journal of Cancer, Vol. 73, Issue 12
Timing of breast cancer surgery in relation to menstrual cycle phase: no effect on 3-year prognosis: The ITS Study
journal, December 2007
- Thorpe, H.; Brown, S. R.; Sainsbury, J. R.
- British Journal of Cancer, Vol. 98, Issue 1
A prospective prognostic study of the hormonal milieu at the time of surgery in premenopausal breast carcinoma
journal, January 2001
- Pujol, Pascal; Daures, Jean-Pierre; Brouillet, Jean-Paul
- Cancer, Vol. 91, Issue 10
Estrous influence on surgical cure of a mouse breast cancer.
journal, July 1988
- Ratajczak, H. V.; Sothern, R. B.; Hrushesky, W. J.
- Journal of Experimental Medicine, Vol. 168, Issue 1
Influence of the estrous cycle at gamma-ray exposure on radiation-induced mammary tumorigenesis in virgin rats
journal, September 1992
- Inano, Hiroshi; Ishii-Ohba, Hiroko; Suzuki, Keiko
- International Journal of Cancer, Vol. 52, Issue 3
Cellular Turnover in the Mammary Gland Is Correlated with Systemic Levels of Progesterone and Not 17β-Estradiol During the Estrous Cycle1
journal, September 2001
- Fata, Jimmie E.; Chaudhary, Varun; Khokha, Rama
- Biology of Reproduction, Vol. 65, Issue 3
Estrous Cycle Regulation of Mammary Epithelial Cell Proliferation, Differentiation, and Death in the Sprague-Dawley Rat: A Model for Investigating the Role of Estrous Cycling in Mammary Carcinogenesis
journal, January 2000
- Schedin, P.
- Journal of Mammary Gland Biology and Neoplasia, Vol. 5, Issue 2, p. 211-225
Dual roles for macrophages in ovarian cycle-associated development and remodelling of the mammary gland epithelium
journal, December 2010
- Chua, Angela C. L.; Hodson, Leigh J.; Moldenhauer, Lachlan M.
- Development, Vol. 137, Issue 24
Natural Killer Cell Activity: Age, Estrous-and Circadian-Stage Dependence and Inverse Correlation With Metastatic Potential
journal, October 1988
- Hrushesky, W. J. M.; Gruber, S. A.; Sothern, R. B.
- JNCI Journal of the National Cancer Institute, Vol. 80, Issue 15
The sensitivity of lymphocytes to ionising radiation
journal, October 1952
- Trowell, O. A.
- The Journal of Pathology and Bacteriology, Vol. 64, Issue 4
Breast Cancer After Treatment of Hodgkin's Disease
journal, January 1993
- Hancock, S. L.; Tucker, M. A.; Hoppe, R. T.
- JNCI Journal of the National Cancer Institute, Vol. 85, Issue 1
Breast Neoplasms in Women Treated With X-Rays for Acute Postpartum Mastitis
2
journal, September 1977
- Shore, Roy E.; Hempelmann, Louis H.; Kowaluk, Eugene
- JNCI: Journal of the National Cancer Institute, Vol. 59, Issue 3
Low doses of ionizing radiation induce immune-stimulatory responses in isolated human primary monocytes
journal, September 2013
- El-Saghire, Houssein; Michaux, Arlette; Thierens, Hubert
- International Journal of Molecular Medicine, Vol. 32, Issue 6
Study of antioxidative effects and anti-inflammatory effects in mice due to low-dose X-irradiation or radon inhalation
journal, February 2013
- Kataoka, T.
- Journal of Radiation Research, Vol. 54, Issue 4
Lymphopenia is an Independent Predictor of Inferior Outcome in Clear Cell Renal Carcinoma
journal, February 2013
- Saroha, Sunil; Uzzo, Robert G.; Plimack, Elizabeth R.
- Journal of Urology, Vol. 189, Issue 2
Lymphocyte Counts Independently Predict Overall Survival in Advanced Cancer Patients: A Biomarker for IL-2 Immunotherapy
journal, September 2003
- Fumagalli, Luca A.; Vinke, Jan; Hoff, Wilco
- Journal of Immunotherapy, Vol. 26, Issue 5
Changes in the superoxide radical and superoxide dismutase levels in the uterus of Rattus norvegicus during the estrous cycle and a possible role for superoxide radical in uterine oedema and cell proliferation at proestrus
journal, April 1991
- Laloraya, M.; Kumar, G. P.; Laloraya, M. M.
- Biochemistry and Cell Biology, Vol. 69, Issue 4
Metabolic regulation in the lactating mammary gland: a lipid synthesizing machine
journal, February 2007
- Rudolph, Michael C.; McManaman, James L.; Phang, TzuLip
- Physiological Genomics, Vol. 28, Issue 3
Lipid metabolism in the lactating mammary gland
journal, August 1997
- Barber, Michael C.; Clegg, Roger A.; Travers, Maureen T.
- Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 1347, Issue 2-3
Regulation of type I interferon responses
journal, December 2013
- Ivashkiv, Lionel B.; Donlin, Laura T.
- Nature Reviews Immunology, Vol. 14, Issue 1
OASL1 inhibits translation of the type I interferon–regulating transcription factor IRF7
journal, February 2013
- Lee, Myeong Sup; Kim, Byungil; Oh, Goo Taeg
- Nature Immunology, Vol. 14, Issue 4
IRF-7 is the master regulator of type-I interferon-dependent immune responses
journal, March 2005
- Honda, Kenya; Yanai, Hideyuki; Negishi, Hideo
- Nature, Vol. 434, Issue 7034
Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape
journal, July 2012
- Bidwell, Bradley N.; Slaney, Clare Y.; Withana, Nimali P.
- Nature Medicine, Vol. 18, Issue 8
Next-generation transcriptome sequencing of the premenopausal breast epithelium using specimens from a normal human breast tissue bank
journal, March 2014
- Pardo, Ivanesa; Lillemoe, Heather A.; Blosser, Rachel J.
- Breast Cancer Research, Vol. 16, Issue 2
Interferon-ε Protects the Female Reproductive Tract from Viral and Bacterial Infection
journal, March 2013
- Fung, Ka Yee; Mangan, Niamh E.; Cumming, Helen
- Science, Vol. 339, Issue 6123
The A and B isoforms of the human progesterone receptor operate through distinct signaling pathways within target cells.
journal, December 1994
- Wen, D. X.; Xu, Y. F.; Mais, D. E.
- Molecular and Cellular Biology, Vol. 14, Issue 12
Different regions of the estrogen receptor are required for synergistic action with the glucocorticoid and progesterone receptors.
journal, December 1989
- Cato, A. C.; Ponta, H.
- Molecular and Cellular Biology, Vol. 9, Issue 12
Genetic Differences in Transcript Responses to Low-Dose Ionizing Radiation Identify Tissue Functions Associated with Breast Cancer Susceptibility
journal, October 2012
- Snijders, Antoine M.; Marchetti, Francesco; Bhatnagar, Sandhya
- PLoS ONE, Vol. 7, Issue 10
Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression
journal, September 2009
- Fujimoto, Hiroshi; Sangai, Takafumi; Ishii, Genichiro
- International Journal of Cancer, Vol. 125, Issue 6
TNFα acting on TNFR1 promotes breast cancer growth via p42/P44 MAPK, JNK, Akt and NF-κB-dependent pathways
journal, February 2008
- Rivas, Martín A.; Carnevale, Romina P.; Proietti, Cecilia J.
- Experimental Cell Research, Vol. 314, Issue 3
Eotaxin Is Required for Eosinophil Homing into the Stroma of the Pubertal and Cycling Uterus
journal, October 2001
- Gouon-Evans, Valérie; Pollard, Jeffrey W.
- Endocrinology, Vol. 142, Issue 10
Direct Intratumoral Injection of an Adenovirus Expressing Interleukin-12 Induces Regression and Long-Lasting Immunity That Is Associated with Highly Localized Expression of Interleukin-12
journal, October 1996
- Bramson, J. L.; Hitt, M.; Addison, C. L.
- Human Gene Therapy, Vol. 7, Issue 16
Adaptive immunity maintains occult cancer in an equilibrium state
journal, November 2007
- Koebel, Catherine M.; Vermi, William; Swann, Jeremy B.
- Nature, Vol. 450, Issue 7171
IFN-α and IL-12 activate IFN regulatory factor 1 (IRF-1), IRF-4, and IRF-8 gene expression in human NK and T cells
journal, November 2003
- Lehtonen, Anne; Lund, Riikka; Lahesmaa, Riitta
- Cytokine, Vol. 24, Issue 3
Interleukin 12–mediated Prevention of Spontaneous Mammary Adenocarcinomas in Two Lines of Her-2/neu Transgenic Mice
journal, August 1998
- Boggio, Katia; Nicoletti, Giordano; Di Carlo, Emma
- Journal of Experimental Medicine, Vol. 188, Issue 3
Candidate Genes Associated with Tumor Regression Mediated by Intratumoral Il-12 Electroporation Gene Therapy
journal, March 2004
- Li, Shulin; Xia, Xueqing; Mellieon, Francesca M.
- Molecular Therapy, Vol. 9, Issue 3
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013
- Kim, Daehwan; Pertea, Geo; Trapnell, Cole
- Genome Biology, Vol. 14, Issue 4
Comparison of Four Nuclear Isolation Buffers for Plant DNA Flow Cytometry
journal, July 2006
- Loureiro, JoÃO; Rodriguez, Eleazar; DoleŽEl, Jaroslav
- Annals of Botany, Vol. 98, Issue 3
Finding consistent patterns: A nonparametric approach for identifying differential expression in RNA-Seq data
journal, November 2011
- Li, Jun; Tibshirani, Robert
- Statistical Methods in Medical Research, Vol. 22, Issue 5
Differential expression analysis for sequence count data
journal, October 2010
- Anders, Simon; Huber, Wolfgang
- Genome Biology, Vol. 11, Issue 10
Definition of Clinically Distinct Molecular Subtypes in Estrogen Receptor–Positive Breast Carcinomas Through Genomic Grade
journal, April 2007
- Loi, Sherene; Haibe-Kains, Benjamin; Desmedt, Christine
- Journal of Clinical Oncology, Vol. 25, Issue 10
Works referencing / citing this record:
Transcriptional repression of IFNβ1 by ATF2 confers melanoma resistance to therapy
journal, March 2015
- Lau, E.; Sedy, J.; Sander, C.
- Oncogene, Vol. 34, Issue 46
A generic cycling hypoxia-derived prognostic gene signature: application to breast cancer profiling
journal, July 2014
- Boidot, Romain; Branders, Samuel; Helleputte, Thibault
- Oncotarget, Vol. 5, Issue 16
Therapeutic targeting of macrophages enhances chemotherapy efficacy by unleashing type I interferon response
journal, March 2019
- Salvagno, Camilla; Ciampricotti, Metamia; Tuit, Sander
- Nature Cell Biology, Vol. 21, Issue 4
Conservation of immune gene signatures in solid tumors and prognostic implications
journal, November 2016
- Chifman, Julia; Pullikuth, Ashok; Chou, Jeff W.
- BMC Cancer, Vol. 16, Issue 1
Diverse tumour susceptibility in Collaborative Cross mice: identification of a new mouse model for human gastric tumourigenesis
journal, March 2019
- Wang, Pin; Wang, Yunshan; Langley, Sasha A.
- Gut, Vol. 68, Issue 11
Therapeutic targeting of macrophages enhances chemotherapy efficacy by unleashing type I interferon response
journal, March 2019
- Salvagno, Camilla; Ciampricotti, Metamia; Tuit, Sander
- Nature Cell Biology, Vol. 21, Issue 4
Two-Tier Mapper, an unbiased topology-based clustering method for enhanced global gene expression analysis
journal, February 2019
- Jeitziner, Rachel; Carrière, Mathieu; Rougemont, Jacques
- Bioinformatics, Vol. 35, Issue 18
Type I interferons in anticancer immunity
journal, June 2015
- Zitvogel, Laurence; Galluzzi, Lorenzo; Kepp, Oliver
- Nature Reviews Immunology, Vol. 15, Issue 7
Diverse tumour susceptibility in Collaborative Cross mice: identification of a new mouse model for human gastric tumourigenesis
journal, March 2019
- Wang, Pin; Wang, Yunshan; Langley, Sasha A.
- Gut, Vol. 68, Issue 11
Genetic Background Modulates lncRNA-Coordinated Tissue Response to Low Dose Ionizing Radiation
journal, January 2015
- Tang, Jonathan; Huang, Yurong; Nguyen, David H.
- International Journal of Genomics, Vol. 2015
Transcriptional repression of IFNβ1 by ATF2 confers melanoma resistance to therapy
journal, March 2015
- Lau, E.; Sedy, J.; Sander, C.
- Oncogene, Vol. 34, Issue 46
Individual variations in dose response for spatial memory learning among outbred wistar rats exposed from 5 to 20 cGy of 56 Fe particles: Individual Variation in Dose Response for Learning
journal, May 2016
- Wyrobek, Andrew J.; Britten, Richard A.
- Environmental and Molecular Mutagenesis, Vol. 57, Issue 5
Conservation of immune gene signatures in solid tumors and prognostic implications
journal, November 2016
- Chifman, Julia; Pullikuth, Ashok; Chou, Jeff W.
- BMC Cancer, Vol. 16, Issue 1
Genetic Background Modulates lncRNA-Coordinated Tissue Response to Low Dose Ionizing Radiation
journal, January 2015
- Tang, Jonathan; Huang, Yurong; Nguyen, David H.
- International Journal of Genomics, Vol. 2015