Inflammaging is associated with shifted macrophage ontogeny and polarization in the aging mouse ovary

in Reproduction
Authors:
Zijing Zhang Department of Obstetrics and Gynecology, Division of Research, Women & Infants Hospital of Rhode Island, Providence, Rhode Island, USA

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Florencia Schlamp Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, USA

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Lu Huang Department of Microbiology and immunology, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA

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Haley Clark Department of Obstetrics and Gynecology, Division of Research, Women & Infants Hospital of Rhode Island, Providence, Rhode Island, USA

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Lynae Brayboy Department of Obstetrics and Gynecology, Division of Research, Women & Infants Hospital of Rhode Island, Providence, Rhode Island, USA
Department of Obstetrics and Gynecology, Division of Reproductive Endocrinology and Infertility, Women & Infants Hospital of Rhode Island, Providence, Rhode Island, USA
Alpert Medical School of Brown University, Providence, Rhode Island, USA
Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, Rhode Island, USA

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Correspondence should be addressed to L Brayboy; Email: Lynae_brayboy@brown.edu
DOI:
https://doi.org/10.1530/REP-19-0330
Volume/Issue:
Volume 159: Issue 3
Page Range:
325–337
Article Type:
Research Article
Online Publication Date:
Mar 2020
Copyright:
© 2020 Society for Reproduction and Fertility 2020
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The fertility of women declines sharply after age 35 and is essentially lost upon menopause at age 51. The ovary plays an important part in aging-associated changes in women’s physiology since it is an essential component of both the reproductive and endocrine systems. Several previous studies in mice have shown that the ovarian tissue goes through drastic changes over the course of aging and exhibits signs of aging-associated chronic inflammation (inflammaging), which may contribute to the marked decline of oocyte quality in aged individuals. To further examine aging-associated gene expression changes in the ovary and to characterize the development of inflammaging, we performed detailed transcriptomic analysis of whole ovaries from mice of six different age groups over the mouse reproductive lifespan and identified more than 5000 genes with significant expression change over the course of aging. Intriguingly, we found aging-associated changes in the expression of several markers that indicate alterations in the composition of ovarian macrophages, which are known to be central players of inflammaging. Using flow cytometry, we analyzed and compared macrophage populations and polarization in young and old ovaries and found a significant increase in monocyte recruitment and macrophage alternative activation (M2) in the old ovaries compared to those in young. Our results are consistent with previous findings of aging-associated increase of fibrosis in the ovarian stromal extracellular matrix, and they provide new clues about the development of inflammaging in the mammalian ovary.

Supplementary Materials

    • Table S1 All normalized gene read counts of the 18 samples.
    • Table S2 Fitness of all differentially expressed genes to a linear or quadratic model.

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Allen JE & Wynn TA 2011 Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathogens e1002003. (https://doi.org/10.1371/journal.ppat.1002003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Banerjee J, Sharma R, Agarwal A, Maitra D, Diamond MP & Abu-Soud HM 2012 IL-6 and mouse oocyte spindle. PLoS ONE e35535. (https://doi.org/10.1371/journal.pone.0035535)

  • Briley SM, Jasti S, Mccracken JM, Hornick JE, Fegley B, Pritchard MT & Duncan FE 2016 Reproductive age-associated fibrosis in the stroma of the mammalian ovary. Reproduction 245–260. (https://doi.org/10.1530/REP-16-0129)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Care AS, Diener KR, Jasper MJ, Brown HM, Ingman WV & Robertson SA 2013 Macrophages regulate corpus luteum development during embryo implantation in mice. Journal of Clinical Investigation 3472–3487. (https://doi.org/10.1172/JCI60561)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chavez-Galan L, Olleros ML, Vesin D & Garcia I 2015 Much more than M1 and M2 macrophages, there are also CD169(+) and TCR(+) macrophages. Frontiers in Immunology 263. (https://doi.org/10.3389/fimmu.2015.00263)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cheng H, Wang Z, Fu L & Xu T 2019 Macrophage polarization in the development and progression of ovarian cancers: an overview. Frontiers in Oncology 421. (https://doi.org/10.3389/fonc.2019.00421)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chiang T, Duncan FE, Schindler K, Schultz RM & Lampson MA 2010 Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Current Biology 1522–1528. (https://doi.org/10.1016/j.cub.2010.06.069)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Colotta F, Allavena P, Sica A, Garlanda C & Mantovani A 2009 Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 1073–1081. (https://doi.org/10.1093/carcin/bgp127)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cruz-Guilloty F, Saeed AM, Echegaray JJ, Duffort S, Ballmick A, Tan Y, Betancourt M, Viteri E, Ramkhellawan GC & Ewald E et al.2013 Infiltration of proinflammatory m1 macrophages into the outer retina precedes damage in a mouse model of age-related macular degeneration. International Journal of Inflammation 503725. (https://doi.org/10.1155/2013/503725)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Daniel JM 2013 Estrogens, estrogen receptors, and female cognitive aging: the impact of timing. Hormones and Behavior 231–237. (https://doi.org/10.1016/j.yhbeh.2012.05.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Doherty TM, Kastelein R, Menon S, Andrade S & Coffman RL 1993 Modulation of murine macrophage function by IL-13. Journal of Immunology 7151–7160.

  • Doyle AG, Herbein G, Montaner LJ, Minty AJ, Caput D, Ferrara P & Gordon S 1994 Interleukin-13 alters the activation state of murine macrophages in vitro: comparison with interleukin-4 and interferon-gamma. European Journal of Immunology 1441–1445. (https://doi.org/10.1002/eji.1830240630)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Duncan FE, Jasti S, Paulson A, Kelsh JM, Fegley B & Gerton JL 2017 Age-associated dysregulation of protein metabolism in the mammalian oocyte. Aging Cell 1381–1393. (https://doi.org/10.1111/acel.12676)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Eastman AJ, He X, Qiu Y, Davis MJ, Vedula P, Lyons DM, Park YD, Hardison SE, Malachowski AN & Osterholzer JJ et al.2015 Cryptococcal heat shock protein 70 homolog Ssa1 contributes to pulmonary expansion of Cryptococcus neoformans during the afferent phase of the immune response by promoting macrophage M2 polarization. Journal of Immunology 5999–6010. (https://doi.org/10.4049/jimmunol.1402719)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Efron B & Tibshirani R 2007 On testing the significance of sets of genes. Annals of Applied Statistics 107–129. (https://doi.org/10.1214/07-AOAS101)

  • Ferrucci L, Corsi A, Lauretani F, Bandinelli S, Bartali B, Taub DD, Guralnik JM & Longo DL 2005 The origins of age-related proinflammatory state. Blood 2294–2299. (https://doi.org/10.1182/blood-2004-07-2599)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Franceschi C & Campisi J 2014 Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. Journals of Gerontology (Supplement 1) S4–S9. (https://doi.org/10.1093/gerona/glu057)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Franceschi C, Garagnani P, Vitale G, Capri M & Salvioli S 2017 Inflammaging and ‘garb-aging’. Trends in Endocrinology and Metabolism 199–212. (https://doi.org/10.1016/j.tem.2016.09.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fukumatsu Y, Katabuchi H, Naito M, Takeya M, Takahashi K & Okamura H 1992 Effect of macrophages on proliferation of granulosa cells in the ovary in rats. Journal of Reproduction and Fertility 241–249. (https://doi.org/10.1530/jrf.0.0960241)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fulop T, Larbi A, Dupuis G, Le Page A, Frost EH, Cohen AA, Witkowski JM & Franceschi C 2017 Immunosenescence and inflamm-aging as two sides of the same coin: friends or foes? Frontiers in Immunology 1960. (https://doi.org/10.3389/fimmu.2017.01960)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG & Gordonov S et al.2012 Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nature Immunology 1118–1128. (https://doi.org/10.1038/ni.2419)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ge J, Li C, Li C, Huang Z, Zeng J, Han L & Wang Q 2019 SIRT6 participates in the quality control of aged oocytes via modulating telomere function. Aging 1965–1976. (https://doi.org/10.18632/aging.101885)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Germano G, Allavena P & Mantovani A 2008 Cytokines as a key component of cancer-related inflammation. Cytokine 374–379. (https://doi.org/10.1016/j.cyto.2008.07.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Goh YP, Henderson NC, Heredia JE, Red Eagle A, Odegaard JI, Lehwald N, Nguyen KD, Sheppard D, Mukundan L & Locksley RM et al.2013 Eosinophils secrete IL-4 to facilitate liver regeneration. PNAS 9914–9919. (https://doi.org/10.1073/pnas.1304046110)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gordon S & Taylor PR 2005 Monocyte and macrophage heterogeneity. Nature Reviews: Immunology 953–964. (https://doi.org/10.1038/nri1733)

  • Grondahl ML, Yding Andersen C, Bogstad J, Nielsen FC, Meinertz H & Borup R 2010 Gene expression profiles of single human mature oocytes in relation to age. Human Reproduction 957–968. (https://doi.org/10.1093/humrep/deq014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J & Lucas D et al.2013 Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 792–804. (https://doi.org/10.1016/j.immuni.2013.04.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heffner LJ 2004 Advanced maternal age--how old is too old? New England Journal of Medicine 1927–1929. (https://doi.org/10.1056/NEJMp048087)

  • Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC, Locksley RM, Rando TA & Chawla A 2013 Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 376–388. (https://doi.org/10.1016/j.cell.2013.02.053)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hornick JE, Duncan FE, Sun M, Kawamura R, Marko JF & Woodruff TK 2015 Age-associated alterations in the micromechanical properties of chromosomes in the mammalian egg. Journal of Assisted Reproduction and Genetics 765–769. (https://doi.org/10.1007/s10815-015-0453-y)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Huang L & Appleton JA 2016 Eosinophils in helminth infection: defenders and dupes. Trends in Parasitology 798–807. (https://doi.org/10.1016/j.pt.2016.05.004)

  • Huang L, Nazarova EV, Tan S, Liu Y & Russell DG 2018 Growth of Mycobacterium tuberculosis in vivo segregates with host macrophage metabolism and ontogeny. Journal of Experimental Medicine 1135–1152. (https://doi.org/10.1084/jem.20172020)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Italiani P & Boraschi D 2014 From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Frontiers in Immunology 514. (https://doi.org/10.3389/fimmu.2014.00514)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, Van Rooijen N, Macdonald AS & Allen JE 2011 Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 1284–1288. (https://doi.org/10.1126/science.1204351)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jenkins SJ, Ruckerl D, Thomas GD, Hewitson JP, Duncan S, Brombacher F, Maizels RM, Hume DA & Allen JE 2013 IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. Journal of Experimental Medicine 2477–2491. (https://doi.org/10.1084/jem.20121999)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Johnson JA & Tough S 2017 No-271-delayed child-bearing. Journal of Obstetrics and Gynaecology Canada e500–e515. (https://doi.org/10.1016/j.jogc.2017.09.007)

  • Jones KT & Lane SI 2013 Molecular causes of aneuploidy in mammalian eggs. Development 3719–3730. (https://doi.org/10.1242/dev.090589)

  • Kennedy BK, Berger SL, Brunet A, Campisi J, Cuervo AM, Epel ES, Franceschi C, Lithgow GJ, Morimoto RI & Pessin JE et al.2014 Geroscience: linking aging to chronic disease. Cell 709–713. (https://doi.org/10.1016/j.cell.2014.10.039)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kumar BV, Connors TJ & Farber DL 2018 Human T cell development, localization, and function throughout life. Immunity 202–213. (https://doi.org/10.1016/j.immuni.2018.01.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lagasse E & Weissman IL 1996 Flow cytometric identification of murine neutrophils and monocytes. Journal of Immunological Methods 139–150. (https://doi.org/10.1016/0022-1759(96)00138-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lambert KC, Curran EM, Judy BM, Lubahn DB & Estes DM 2004 Estrogen receptor-alpha deficiency promotes increased TNF-alpha secretion and bacterial killing by murine macrophages in response to microbial stimuli in vitro. Journal of Leukocyte Biology 1166–1172. (https://doi.org/10.1189/jlb.1103589)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lavin Y, Mortha A, Rahman A & Merad M 2015 Regulation of macrophage development and function in peripheral tissues. Nature Reviews: Immunology 731–744. (https://doi.org/10.1038/nri3920)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Love MI, Huber W & Anders S 2014 Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 550. (https://doi.org/10.1186/s13059-014-0550-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lupardus PJ, Birnbaum ME & Garcia KC 2010 Molecular basis for shared cytokine recognition revealed in the structure of an unusually high affinity complex between IL-13 and IL-13Ralpha2. Structure 332–342. (https://doi.org/10.1016/j.str.2010.01.003)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mantovani A, Allavena P, Sica A & Balkwill F 2008 Cancer-related inflammation. Nature 436–444. (https://doi.org/10.1038/nature07205)

  • Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D & Thomas PD 2017 PANTHER version 11: expanded annotation data from gene ontology and reactome pathways, and data analysis tool enhancements. Nucleic Acids Research D183–D189. (https://doi.org/10.1093/nar/gkw1138)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mi H, Muruganujan A, Ebert D, Huang X & Thomas PD 2019 PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Research D419–D426. (https://doi.org/10.1093/nar/gky1038)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mills CD, Kincaid K, Alt JM, Heilman MJ & Hill AM 2000 M-1/M-2 macrophages and the Th1/Th2 paradigm. Journal of Immunology 6166–6173. (https://doi.org/10.4049/jimmunol.164.12.6166)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Moley KH & Schreiber JR 1995 Ovarian follicular growth, ovulation and atresia. Endocrine, paracrine and autocrine regulation. Advances in Experimental Medicine and Biology 103–119. (https://doi.org/10.1007/978-1-4899-0952-7_7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mueller SN & Mackay LK 2016 Tissue-resident memory T cells: local specialists in immune defence. Nature Reviews: Immunology 79–89. (https://doi.org/10.1038/nri.2015.3)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nelson JF, Felicio LS, Randall PK, Sims C & Finch CE 1982 A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology. Biology of Reproduction 327–339. (https://doi.org/10.1095/biolreprod27.2.327)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nteeba J, Ganesan S & Keating AF 2014 Progressive obesity alters ovarian folliculogenesis with impacts on pro-inflammatory and steroidogenic signaling in female mice. Biology of Reproduction 86. (https://doi.org/10.1095/biolreprod.114.121343)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parihar A, Eubank TD & Doseff AI 2010 Monocytes and macrophages regulate immunity through dynamic networks of survival and cell death. Journal of Innate Immunity 204–215. (https://doi.org/10.1159/000296507)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pepe G, Braga D, Renzi TA, Villa A, Bolego C, D'avila F, Barlassina C, Maggi A, Locati M & Vegeto E 2017 Self-renewal and phenotypic conversion are the main physiological responses of macrophages to the endogenous estrogen surge. Scientific Reports 44270. (https://doi.org/10.1038/srep44270)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pepe G, Locati M, Della Torre S, Mornata F, Cignarella A, Maggi A & Vegeto E 2018 The estrogen-macrophage interplay in the homeostasis of the female reproductive tract. Human Reproduction Update 652–672. (https://doi.org/10.1093/humupd/dmy026)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pine GM, Batugedara HM & Nair MG 2018 Here, there and everywhere: resistin-like molecules in infection, inflammation, and metabolic disorders. Cytokine 442–451. (https://doi.org/10.1016/j.cyto.2018.05.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Raggi F, Pelassa S, Pierobon D, Penco F, Gattorno M, Novelli F, Eva A, Varesio L, Giovarelli M & Bosco MC 2017 Regulation of human macrophage M1-M2 polarization balance by hypoxia and the triggering receptor expressed on myeloid Cells-1. Frontiers in Immunology 1097. (https://doi.org/10.3389/fimmu.2017.01097)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Reidy PT, Mckenzie AI, Mahmassani ZS, Petrocelli JJ, Nelson DB, Lindsay CC, Gardner JE, Morrow VR, Keefe AC & Huffaker TB et al.2019 Aging impairs mouse skeletal muscle macrophage polarization and muscle-specific abundance during recovery from disuse. American Journal of Physiology: Endocrinology and Metabolism E85–E98. (https://doi.org/10.1152/ajpendo.00422.2018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Richards JS, Russell DL, Ochsner S, Hsieh M, Doyle KH, Falender AE, Lo YK & Sharma SC 2002 Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Progress in Hormone Research 195–220. (https://doi.org/10.1210/rp.57.1.195)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rosenberg HF, Dyer KD & Foster PS 2013 Eosinophils: changing perspectives in health and disease. Nature Reviews: Immunology 9–22. (https://doi.org/10.1038/nri3341)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Russell DG, Huang L & Vanderven BC 2019 Immunometabolism at the interface between macrophages and pathogens. Nature Reviews: Immunology 291–304. (https://doi.org/10.1038/s41577-019-0124-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Salam N, Rane S, Das R, Faulkner M, Gund R, Kandpal U, Lewis V, Mattoo H, Prabhu S & Ranganathan V et al.2013 T cell ageing: effects of age on development, survival & function. Indian Journal of Medical Research 595–608.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Salvioli S, Monti D, Lanzarini C, Conte M, Pirazzini C, Bacalini MG, Garagnani P, Giuliani C, Fontanesi E & Ostan R et al.2013 Immune system, cell senescence, aging and longevity--inflamm-aging reappraised. Current Pharmaceutical Design 1675–1679. (https://doi.org/10.2174/138161213805219531)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Saule P, Trauet J, Dutriez V, Lekeux V, Dessaint JP & Labalette M 2006 Accumulation of memory T cells from childhood to old age: central and effector memory cells in CD4(+) versus effector memory and terminally differentiated memory cells in CD8(+) compartment. Mechanisms of Ageing and Development 274–281. (https://doi.org/10.1016/j.mad.2005.11.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shi C & Pamer EG 2011 Monocyte recruitment during infection and inflammation. Nature Reviews: Immunology 762–774. (https://doi.org/10.1038/nri3070)

  • Skaznik-Wikiel ME, Swindle DC, Allshouse AA, Polotsky AJ & McManaman JL 2016 High-fat diet causes subfertility and compromised ovarian function independent of obesity in mice. Biology of Reproduction 108. (https://doi.org/10.1095/biolreprod.115.137414)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Snider AP & Wood JR 2019 Obesity induces ovarian inflammation and reduces oocyte quality. Reproduction 158 R79–R90. (https://doi.org/10.1530/REP-18-0583)

  • Stein M, Keshav S, Harris N & Gordon S 1992 Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. Journal of Experimental Medicine 287–292. (https://doi.org/10.1084/jem.176.1.287)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Thomas FH & Vanderhyden BC 2006 Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reproductive Biology and Endocrinology 19. (https://doi.org/10.1186/1477-7827-4-19)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan WC & Fraser HM 2011 Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction 821–831. (https://doi.org/10.1530/REP-10-0327)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Van Dyken SJ & Locksley RM 2013 Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annual Review of Immunology 317–343. (https://doi.org/10.1146/annurev-immunol-032712-095906)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Van Kempen TA, Milner TA & Waters EM 2011 Accelerated ovarian failure: a novel, chemically induced animal model of menopause. Brain Research 176–187. (https://doi.org/10.1016/j.brainres.2010.12.064)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wise PM, Smith MJ, Dubal DB, Wilson ME, Rau SW, Cashion AB, Bottner M & Rosewell KL 2002 Neuroendocrine modulation and repercussions of female reproductive aging. Recent Progress in Hormone Research 235–256. (https://doi.org/10.1210/rp.57.1.235)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wood N, Whitters MJ, Jacobson BA, Witek J, Sypek JP, Kasaian M, Eppihimer MJ, Unger M, Tanaka T & Goldman SJ et al.2003 Enhanced interleukin (IL)-13 responses in mice lacking IL-13 receptor alpha 2. Journal of Experimental Medicine 703–709. (https://doi.org/10.1084/jem.20020906)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A & Locksley RM 2011 Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 243–247. (https://doi.org/10.1126/science.1201475)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wu R, Van Der Hoek KH, Ryan NK, Norman RJ & Robker RL 2004 Macrophage contributions to ovarian function. Human Reproduction Update 119–133. (https://doi.org/10.1093/humupd/dmh011)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wynn TA & Vannella KM 2016 Macrophages in tissue repair, regeneration, and fibrosis. Immunity 450–462. (https://doi.org/10.1016/j.immuni.2016.02.015)

  • Yu W, Chen J, Xiong Y, Pixley FJ, Yeung YG & Stanley ER 2012 Macrophage proliferation is regulated through CSF-1 receptor tyrosines 544, 559, and 807. Journal of Biological Chemistry 13694–13704. (https://doi.org/10.1074/jbc.M112.355610)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhao Y, Zou W, Du J & Zhao Y 2018 The origins and homeostasis of monocytes and tissue-resident macrophages in physiological situation. Journal of Cellular Physiology 6425–6439. (https://doi.org/10.1002/jcp.26461)

    • PubMed
    • Search Google Scholar
    • Export Citation