Generic placeholder image

Current Aging Science

Editor-in-Chief

ISSN (Print): 1874-6098
ISSN (Online): 1874-6128

Review Article

Inflammaging of Female Reproductive System: A Molecular Landscape

Author(s): Valeriia Rodichkina*, Igor Kvetnoy, Victoria Polyakova, Alexander Arutjunyan, Ruslan Nasyrov and Dmitry Ivanov

Volume 14, Issue 1, 2021

Published on: 29 September, 2020

Page: [10 - 18] Pages: 9

DOI: 10.2174/1874609813666200929112624

Price: $65

Abstract

Aging is a complex biological process, a major aspect of which is the accumulation of somatic changes throughout life. Cellular senescence is a condition in which cells undergo an irreversible cell cycle arrest in response to various cellular stresses. Once the cells begin to senesce, they become more resistant to any mutagens, including oncogenic factors. Inflammaging (inflammatory aging) is an age-related, chronic, and systemic inflammatory condition realized by cells with the Senescence-Associated Secretory Phenotype (SASP). These recently recognized senescent phenotypes associated with aging have been reported to promote better wound healing, embryonic development, as well as stimulation and extension of the tumor process. It is assumed that cellular senescence contributes to the age-related decline of reproductive function due to the association of senescent cells with aging and age-related diseases. Thus, SASPs have both positive and negative effects, depending on the biological context. SASP cell accumulation in tissues contributes to an age-related functional decline of the tissue and organ state. In this review, the term “cellular senescence” is used to refer to the processes of cells irreversible growth inhibition during their viable state, while the term “aging” is used to indicate the deterioration of tissues due to loss of function. Late reproductive age is associated with infertility and possible complications of the onset and maintenance of pregnancy. Senescent cells express pro-inflammatory cytokines, growth factors, and matrix metalloproteinases and some other molecules collectively called the Senescence-Associated Secretory Phenotype (SASP).

Keywords: Aging, inflammaging, ovary, corpus luteum, fallopian tubes, uterus.

Graphical Abstract
[1]
Baker DJ, Childs BG, Durik M, et al. Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan. Nature 2016; 530(7589): 184-9.
[http://dx.doi.org/10.1038/nature16932] [PMID: 26840489]
[2]
Stoop D, Cobo A, Silber S. Fertility preservation for age-related fertility decline. Lancet 2014; 384(9950): 1311-9.
[http://dx.doi.org/10.1016/S0140-6736(14)61261-7] [PMID: 25283572]
[3]
Meldrum DR, Casper RF, Diez-Juan A, Simon C, Domar AD, Frydman R. Aging and the environment affect gamete and embryo potential: can we intervene? Fertil Steril 2016; 105(3): 548-59.
[http://dx.doi.org/10.1016/j.fertnstert.2016.01.013] [PMID: 26812244]
[4]
Franceschi C, Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol A Biol Sci Med Sci 2014; 69(Suppl. 1): S4-9.
[http://dx.doi.org/10.1093/gerona/glu057] [PMID: 24833586]
[5]
Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965; 37: 614-36.
[http://dx.doi.org/10.1016/0014-4827(65)90211-9] [PMID: 14315085]
[6]
Sousa-Victor P, Gutarra S, García-Prat L, et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 2014; 506(7488): 316-21.
[http://dx.doi.org/10.1038/nature13013] [PMID: 24522534]
[7]
Herbig U, Ferreira M, Condel L, Carey D, Sedivy JM. Cellular senescence in aging primates. Science 2006; 311(5765): 1257.
[http://dx.doi.org/10.1126/science.1122446] [PMID: 16456035]
[8]
Campisi J. Aging, cellular senescence, and cancer. Annual review of physiology 2013; 75(1): 685-705.
[http://dx.doi.org/10.1146/annurev-physiol-030212-183653]
[9]
Allsopp RC, Vaziri H, Patterson C, et al. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci 1992; 89(21): 10114-8.
[http://dx.doi.org/10.1073/pnas.89.21.10114] [PMID: 1438199]
[10]
Kang C, Xu Q, Martin TD, et al. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 2015; 349(6255): 5612.
[http://dx.doi.org/10.1126/science.aaa5612] [PMID: 26404840]
[11]
Wiley CD, Velarde MC, Lecot P, et al. Mitochondrial dysfunction induces senescence with a distinct secretory phenotype. Cell Metab 2016; 23(2): 303-14.
[http://dx.doi.org/10.1016/j.cmet.2015.11.011] [PMID: 26686024]
[12]
Freund A, Laberge RM, Demaria M, Campisi J. Lamin B1 loss is a senescence-associated biomarker. Mol Biol Cell 2012; 23(11): 2066-75.
[http://dx.doi.org/10.1091/mbc.e11-10-0884] [PMID: 22496421]
[13]
Laberge RM, Sun Y, Orjalo AV, et al. MTOR regulates the pro-tumorigenic senescence-associated secretory phenotype by promoting IL1A translation. Nat Cell Biol 2015; 17(8): 1049-61.
[http://dx.doi.org/10.1038/ncb3195] [PMID: 26147250]
[14]
Childs BG, Baker DJ, Kirkland JL, Campisi J, van Deursen JM. Senescence and apoptosis: dueling or complementary cell fates? EMBO Rep 2014; 15(11): 1139-53.
[http://dx.doi.org/10.15252/embr.201439245] [PMID: 25312810]
[15]
Coppé JP, Patil CK, Rodier F, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008; 6(12): 2853-68.
[http://dx.doi.org/10.1371/journal.pbio.0060301] [PMID: 19053174]
[16]
Velarde MC, Menon R. Positive and negative effects of cellular senescence during female reproductive aging and pregnancy. J Endocrinol 2016; 230(2): R59-76.
[http://dx.doi.org/10.1530/JOE-16-0018] [PMID: 27325241]
[17]
Hubackova S, Krejcikova K, Bartek J, Hodny Z. IL1- and TGFβ-Nox4 signaling, oxidative stress and DNA damage response are shared features of replicative, oncogene-induced, and drug-induced paracrine ‘bystander senescence’. Aging 2012; 4(12): 932-51.
[http://dx.doi.org/10.18632/aging.100520] [PMID: 23385065]
[18]
Coppé JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 2010; 5(1): 99-118.
[http://dx.doi.org/10.1146/annurev-pathol-121808-102144] [PMID: 20078217]
[19]
Schmitt CA. Senescence-associated reprogramming promotes cancer stemness. Endocrine Abstracts. BioScientifica 2018; 56(7686): 96.
[20]
Handel MA, Schimenti JC. Genetics of mammalian meiosis: Regulation, dynamics and impact on fertility. Nat Rev Genet 2010; 11(2): 124-36.
[http://dx.doi.org/10.1038/nrg2723] [PMID: 20051984]
[21]
Xu M, Tchkonia T, Ding H, et al. JAK inhibition alleviates the cellular senescence-associated secretory phenotype and frailty in old age. Proc Natl Acad Sci USA 2015; 112(46): E6301-10.
[http://dx.doi.org/10.1073/pnas.1515386112] [PMID: 26578790]
[22]
Levine ME, Lu AT, Chen BH, et al. Menopause accelerates biological aging. Proc Natl Acad Sci USA 2016; 113(33): 9327-32.
[http://dx.doi.org/10.1073/pnas.1604558113] [PMID: 27457926]
[23]
Bromberger JT, Schott LL, Kravitz HM, et al. Longitudinal change in reproductive hormones and depressive symptoms across the menopausal transition: Results from the study of women’s health across the nation (SWAN). Arch Gen Psychiatry 2010; 67(6): 598-607.
[http://dx.doi.org/10.1001/archgenpsychiatry.2010.55] [PMID: 20530009]
[24]
Pelosi E, Forabosco A, Schlessinger D. Genetics of the ovarian reserve. Front Genet 2015; 6: 308.
[http://dx.doi.org/10.3389/fgene.2015.00308] [PMID: 26528328]
[25]
Pellestor F, Andréo B, Arnal F, Humeau C, Demaille J. Maternal aging and chromosomal abnormalities: New data drawn from unfertilized human oocytes. Hum Genet 2003; 112(2): 195-203.
[http://dx.doi.org/10.1007/s00439-002-0852-x] [PMID: 12522562]
[26]
Baker DJ, Wijshake T, Tchkonia T, et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011; 479(7372): 232-6.
[http://dx.doi.org/10.1038/nature10600] [PMID: 22048312]
[27]
Demaria M, Ohtani N, Youssef SA, et al. An essential role for senescent cells in optimal wound healing through secretion of PDGF-AA. Dev Cell 2014; 31(6): 722-33.
[http://dx.doi.org/10.1016/j.devcel.2014.11.012] [PMID: 25499914]
[28]
Bulmer JN, Lash GE. The role of uterine NK cells in normal reproduction and reproductive disorders. Adv Exp Med Biol 2015; 868: 95-126.
[http://dx.doi.org/10.1007/978-3-319-18881-2_5] [PMID: 26178847]
[29]
Rajagopalan S, Long EO. Cellular senescence induced by CD158d reprograms natural killer cells to promote vascular remodeling. Proc Natl Acad Sci USA 2012; 109(50): 20596-601.
[http://dx.doi.org/10.1073/pnas.1208248109] [PMID: 23184984]
[30]
Menon R, Noda N, Bredeson S, et al. Fetal membranes: Potential source of preterm birth biomarkers.General Meth in Biomarker Res and their App 2015; 1483-529.
[http://dx.doi.org/10.1007/978-94-007-7696-8_28]
[31]
Ishii N, Maruyama N. Biology of aging. Dojin Bioscience Series 2014; pp. 67-83.
[32]
Ferrucci L, Fabbri E. Inflammageing: Chronic inflammation in ageing, cardiovascular disease, and frailty. Nat Rev Cardiol 2018; 15(9): 505-22.
[http://dx.doi.org/10.1038/s41569-018-0064-2] [PMID: 30065258]
[33]
Keefe DL, Liu L, Marquard K. Telomeres and aging-related meiotic dysfunction in women. Cell Mol Life Sci 2007; 64(2): 139-43.
[http://dx.doi.org/10.1007/s00018-006-6466-z] [PMID: 17219022]
[34]
Wilding M. Potential long-term risks associated with maternal aging (the role of the mitochondria). Fertil Steril 2015; 103(6): 1397-401.
[http://dx.doi.org/10.1016/j.fertnstert.2015.03.034] [PMID: 25936236]
[35]
Behnia F, Taylor BD, Woodson M, et al. Chorioamniotic membrane senescence: A signal for parturition. Am J Obstet Gynecol 2015; 213(3): 359-9.
[http://dx.doi.org/10.1016/j.ajog.2015.05.041] [PMID: 26025293]
[36]
Muñoz-Espín D, Cañamero M, Maraver A, et al. Programmed cell senescence during mammalian embryonic development. Cell 2013; 155(5): 1104-18.
[http://dx.doi.org/10.1016/j.cell.2013.10.019] [PMID: 24238962]
[37]
Storer M, Mas A, Robert-Moreno A, et al. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 2013; 155(5): 1119-30.
[http://dx.doi.org/10.1016/j.cell.2013.10.041] [PMID: 24238961]
[38]
Yuan W, Giudice LC. Programmed cell death in human ovary is a function of follicle and corpus luteum status. J Clin Endocrinol Metab 1997; 82(9): 3148-55.
[http://dx.doi.org/10.1210/jc.82.9.3148] [PMID: 9284760]
[39]
Hart EC, Charkoudian N, Miller VM. Sex, hormones and neuroeffector mechanisms. Acta Physiol (Oxf) 2011; 203(1): 155-65.
[http://dx.doi.org/10.1111/j.1748-1716.2010.02192.x] [PMID: 20874808]
[40]
Gunten A, Clerc M, Tomar R, et al. Evolutionary considerations on aging and alzheimer’s disease. J Alzheimers Dis Parkinsonism 2018; 8(1): 423.
[http://dx.doi.org/10.4172/2161-0460.1000423]
[41]
Liu CM, Ding LJ, Li JY, Dai JW, Sun HX. [Advances in the study of ovarian dysfunction with aging]. Yi Chuan 2019; 41(9): 816-26.
[PMID: 31549680]
[42]
Finch CE. The menopause and aging, a comparative perspective. J Steroid Biochem Mol Biol 2014; 142: 132-41.
[http://dx.doi.org/10.1016/j.jsbmb.2013.03.010] [PMID: 23583565]
[43]
Tiwari M, Prasad S, Tripathi A, et al. Apoptosis in mammalian oocytes: A review. Apoptosis 2015; 20(8): 1019-25.
[http://dx.doi.org/10.1007/s10495-015-1136-y] [PMID: 25958165]
[44]
Zhang H, Panula S, Petropoulos S, et al. Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells. Nat Med 2015; 21(10): 1116-8.
[http://dx.doi.org/10.1038/nm.3775] [PMID: 26444631]
[45]
Dunson DB, Baird DD, Colombo B. Increased infertility with age in men and women. Obstet Gynecol 2004; 103(1): 51-6.
[http://dx.doi.org/10.1097/01.AOG.0000100153.24061.45] [PMID: 14704244]
[46]
Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: Mechanisms and new insights into an age-old problem. Nat Rev Genet 2012; 13(7): 493-504.
[http://dx.doi.org/10.1038/nrg3245] [PMID: 22705668]
[47]
Keefe DL, Franco S, Liu L, et al. Telomere length predicts embryo fragmentation after in vitro fertilization in women--toward a telomere theory of reproductive aging in women. Am J Obstet Gynecol 2005; 192(4): 1256-60.
[http://dx.doi.org/10.1016/j.ajog.2005.01.036] [PMID: 15846215]
[48]
Liu L, Franco S, Spyropoulos B, Moens PB, Blasco MA, Keefe DL. Irregular telomeres impair meiotic synapsis and recombination in mice. Proc Natl Acad Sci USA 2004; 101(17): 6496-501.
[http://dx.doi.org/10.1073/pnas.0400755101] [PMID: 15084742]
[49]
Grive KJ, Freiman RN. The developmental origins of the mammalian ovarian reserve. Development 2015; 142(15): 2554-63.
[http://dx.doi.org/10.1242/dev.125211] [PMID: 26243868]
[50]
Costa JJN, Souza GB, Soares MAA, Ribeiro RP, van den Hurk R, Silva JRV. In vitro differentiation of primordial germ cells and oocyte-like cells from stem cells. Histol Histopathol 2018; 33(2): 121-32.
[PMID: 28691729]
[51]
Butts S, Riethman H, Ratcliffe S, Shaunik A, Coutifaris C, Barnhart K. Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab 2009; 94(12): 4835-43.
[http://dx.doi.org/10.1210/jc.2008-2269] [PMID: 19864453]
[52]
Cheng EH, Chen SU, Lee TH, et al. Evaluation of telomere length in cumulus cells as a potential biomarker of oocyte and embryo quality. Hum Reprod 2013; 28(4): 929-36.
[http://dx.doi.org/10.1093/humrep/det004] [PMID: 23377770]
[53]
Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: Regulation by survival and death of granulosa cells. J Reprod Dev 2012; 58(1): 44-50.
[http://dx.doi.org/10.1262/jrd.2011-012] [PMID: 22450284]
[54]
Tsiligiannis S, Panay N, Stevenson JC. Premature Ovarian Insufficiency and Long-Term Health Consequences. Curr Vasc Pharmacol 2019; 17(6): 604-9.
[http://dx.doi.org/10.2174/1570161117666190122101611] [PMID: 30819073]
[55]
Yeganeh L, Boyle JA, Wood A, Teede H, Vincent AJ. Menopause guideline appraisal and algorithm development for premature ovarian insufficiency. Maturitas 2019; 130: 21-31.
[http://dx.doi.org/10.1016/j.maturitas.2019.09.009] [PMID: 31706432]
[56]
Eastell R. Management of osteoporosis due to ovarian failure. Med Pediatr Oncol 2003; 41(3): 222-7.
[http://dx.doi.org/10.1002/mpo.10341] [PMID: 12868123]
[57]
Podfigurna A, Męczekalski B. Cardiovascular health in patients with premature ovarian insufficiency. Management of long-term consequences. Przegl Menopauz 2018; 17(3): 109-11.
[http://dx.doi.org/10.5114/pm.2018.78551] [PMID: 30357009]
[58]
Santoro N. Symptoms of menopause: hot flushes. Clin Obstet Gynecol 2008; 51(3): 539-48.
[http://dx.doi.org/10.1097/GRF.0b013e31818093f6] [PMID: 18677148]
[59]
Hawkes K, Smith KR. Brief communication: Evaluating grandmother effects. Am J Phys Anthropol 2009; 140(1): 173-6.
[http://dx.doi.org/10.1002/ajpa.21061] [PMID: 19373844]
[60]
Nelson SM, Lawlor DA. Predicting live birth, preterm delivery, and low birth weight in infants born from in vitro fertilisation: A prospective study of 144,018 treatment cycles. PLoS Med 2011; 8(1): e1000386.
[http://dx.doi.org/10.1371/journal.pmed.1000386] [PMID: 21245905]
[61]
Magnus MC, Wilcox AJ, Morken NH, Weinberg CR, Håberg SE. Role of maternal age and pregnancy history in risk of miscarriage: Prospective register based study. BMJ 2019; 364: l869.
[http://dx.doi.org/10.1136/bmj.l869] [PMID: 30894356]
[62]
Herbert M, Kalleas D, Cooney D, Lamb M, Lister L. Meiosis and maternal aging: Insights from aneuploid oocytes and trisomy births. Cold Spring Harb Perspect Biol 2015; 7(4): a017970.
[http://dx.doi.org/10.1101/cshperspect.a017970] [PMID: 25833844]
[63]
Tsutsumi M, Fujiwara R, Nishizawa H, et al. Age-related decrease of meiotic cohesins in human oocytes. PLoS One 2014; 9(5): e96710.
[http://dx.doi.org/10.1371/journal.pone.0096710] [PMID: 24806359]
[64]
Tarín JJ, Pérez-Albalá S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod 2001; 65(1): 141-50.
[http://dx.doi.org/10.1095/biolreprod65.1.141] [PMID: 11420234]
[65]
Martin W. Supply and demand of energy in the oocyte and the role of mitochondria. Results Probl Cell Differ 2017; 63: 373-87.
[http://dx.doi.org/10.1007/978-3-319-60855-6_16] [PMID: 28779326]
[66]
Selesniemi K, Lee HJ, Muhlhauser A, et al. Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc Natl Acad Sci 2011; 26;108(30): 12319-24.
[http://dx.doi.org/10.1073/pnas.1018793108]
[67]
Elia EM, Bazzano MV, Quintana R, et al. Reproductive disorders in obesity. Integr Obes Diabetes 2015; 1(1): 20-5.
[68]
Wu LL, Dunning KR, Yang X, et al. High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology 2010; 151(11): 5438-45.
[http://dx.doi.org/10.1210/en.2010-0551] [PMID: 20861227]
[69]
Boots C, Stephenson MD. Does obesity increase the risk of miscarriage in spontaneous conception: A systematic review. Semin Reprod Med 2011; 29(6): 507-13.
[http://dx.doi.org/10.1055/s-0031-1293204] [PMID: 22161463]
[70]
Flenady V, Koopmans L, Middleton P, et al. Major risk factors for stillbirth in high-income countries: A systematic review and meta-analysis. Lancet 2011; 377(9774): 1331-40.
[http://dx.doi.org/10.1016/S0140-6736(10)62233-7] [PMID: 21496916]
[71]
Waldenström U, Cnattingius S, Norman M, Schytt E. Advanced Maternal Age and Stillbirth Risk in Nulliparous and Parous Women. Obstet Gynecol 2015; 126(2): 355-62.
[http://dx.doi.org/10.1097/AOG.0000000000000947] [PMID: 26241426]
[72]
Stubert J, Reister F, Hartmann S, Janni W. The Risks Associated With Obesity in Pregnancy. Dtsch Arztebl Int 2018; 115(16): 276-83.
[http://dx.doi.org/10.3238/arztebl.2018.0276] [PMID: 29739495]
[73]
Lowe WL Jr, Karban J. Genetics, genomics and metabolomics: New insights into maternal metabolism during pregnancy. Diabet Med 2014; 31(3): 254-62.
[http://dx.doi.org/10.1111/dme.12352] [PMID: 24528228]
[74]
Fox R, Kitt J, Leeson P, Aye CYL, Lewandowski AJ. Preeclampsia: Risk factors, diagnosis, management, and the cardiovascular impact on the offspring. J Clin Med 2019; 8(10): 1625.
[http://dx.doi.org/10.3390/jcm8101625] [PMID: 31590294]
[75]
McLennan AS, Gyamfi-Bannerman C, Ananth CV, et al. The role of maternal age in twin pregnancy outcomes. Am J Obstet Gynecol 2017; 217(1): 80-8.
[http://dx.doi.org/10.1016/j.ajog.2017.03.002] [PMID: 28286050]
[76]
Haavaldsen C, Samuelsen SO, Eskild A. The association of maternal age with placental weight: A population-based study of 536,954 pregnancies. BJOG 2011; 118(12): 1470-6.
[http://dx.doi.org/10.1111/j.1471-0528.2011.03053.x] [PMID: 21749632]
[77]
Haavaldsen C, Strøm-Roum EM, Eskild A. Temporal changes in fetal death risk in pregnancies with preeclampsia: Does offspring birthweight matter? A population study. Eur J Obstet Gynecol Reprod Biol X 2019; 2: 100009.
[http://dx.doi.org/10.1016/j.eurox.2019.100009] [PMID: 31396596]
[78]
Yamada Z, Kitagawa M, Takemura T, Hirokawa K. Effect of maternal age on incidences of apoptotic and proliferative cells in trophoblasts of full-term human placenta. Mol Hum Reprod 2001; 7(12): 1179-85.
[http://dx.doi.org/10.1093/molehr/7.12.1179] [PMID: 11719596]
[79]
Bewley S. William Ledger, ‎Dimitrios Nikolaou Reproductive Ageing. London: RSOG press 2009.
[http://dx.doi.org/10.1017/CBO9781107784734]
[80]
Cox LS, Redman C. The role of cellular senescence in ageing of the placenta. Placenta 2017; 52: 139-45.
[http://dx.doi.org/10.1016/j.placenta.2017.01.116] [PMID: 28131318]
[81]
Ubaldi FM, Cimadomo D, Vaiarelli A, et al. Advanced maternal dge in IVF: Still a challenge? The present and the future of its treatment. Front Endocrinol (Lausanne) 2019; 10: 94.
[http://dx.doi.org/10.3389/fendo.2019.00094] [PMID: 30842755]
[82]
Sumeet S, Gurcharan SG, Navjot SG. The impact of uterine therapies on reproductive efficiency in Thoroughbred mares; the possible effect of mare age and reproductive status. Veterenarski arhiv 2011; 81(2): 163-73.
[83]
Shirasuna K, Iwata H. Effect of aging on the female reproductive function. Contracept Reprod Med 2017; 2: 23.
[http://dx.doi.org/10.1186/s40834-017-0050-9] [PMID: 29201428]
[84]
Tanikawa N, Ohtsu A, Kawahara-Miki R, et al. Age-associated mRNA expression changes in bovine endometrial cells in vitro. Reprod Biol Endocrinol 2017; 15(1): 63.
[http://dx.doi.org/10.1186/s12958-017-0284-z] [PMID: 28806906]
[85]
Cano F, Simón C, Remohí J, Pellicer A. Effect of aging on the female reproductive system: Evidence for a role of uterine senescence in the decline in female fecundity. Fertil Steril 1995; 64(3): 584-9.
[http://dx.doi.org/10.1016/S0015-0282(16)57797-8] [PMID: 7543864]
[86]
Baird DD, Weinberg CR, McConnaughey DR, Wilcox AJ. Rescue of the corpus luteum in human pregnancy. Biol Reprod 2003; 68(2): 448-56.
[http://dx.doi.org/10.1095/biolreprod.102.008425] [PMID: 12533407]
[87]
Hirota Y, Daikoku T, Tranguch S, Xie H, Bradshaw HB, Dey SK. Uterine-specific p53 deficiency confers premature uterine senescence and promotes preterm birth in mice. J Clin Invest 2010; 120(3): 803-15.
[http://dx.doi.org/10.1172/JCI40051] [PMID: 20124728]
[88]
Ulbrich SE, Zitta K, Hiendleder S, Wolf E. In vitro systems for intercepting early embryo-maternal cross-talk in the bovine oviduct. Theriogenology 2010; 73(6): 802-16.
[http://dx.doi.org/10.1016/j.theriogenology.2009.09.036] [PMID: 19963260]
[89]
Halbert SA, Tam PY, Blandau RJ. Egg transport in the rabbit oviduct: The roles of cilia and muscle. Science 1976; 191(4231): 1052-3.
[http://dx.doi.org/10.1126/science.1251215] [PMID: 1251215]
[90]
Yan J, Akutsu H, Satoh Y. The morphological and functional observation of the gap junction proteins in the oviduct epithelia in young and adult hamsters. Okajimas Folia Anat Jpn 2011; 88(2): 57-64.
[http://dx.doi.org/10.2535/ofaj.88.57] [PMID: 22184867]
[91]
Tanaka H, Ohtsu A, Shiratsuki S, et al. Age-dependent changes in inflammation and extracellular matrix in bovine oviduct epithelial cells during the post-ovulatory phase. Mol Reprod Dev 2016; 83(9): 815-26.
[http://dx.doi.org/10.1002/mrd.22693] [PMID: 27580129]
[92]
Uri-Belapolsky S, Shaish A, Eliyahu E, et al. Interleukin-1 deficiency prolongs ovarian lifespan in mice. Proc Natl Acad Sci USA 2014; 111(34): 12492-7.
[http://dx.doi.org/10.1073/pnas.1323955111] [PMID: 25114230]
[93]
Clérigues V, Guillén MI, Castejón MA, Gomar F, Mirabet V, Alcaraz MJ. Heme oxygenase-1 mediates protective effects on inflammatory, catabolic and senescence responses induced by interleukin-1β in osteoarthritic osteoblasts. Biochem Pharmacol 2012; 83(3): 395-405.
[http://dx.doi.org/10.1016/j.bcp.2011.11.024] [PMID: 22155307]
[94]
Nelson SM, Telfer EE, Anderson RA. The ageing ovary and uterus: New biological insights. Hum Reprod Update 2013; 19(1): 67-83.
[http://dx.doi.org/10.1093/humupd/dms043] [PMID: 23103636]
[95]
Hasler JF. Forty years of embryo transfer in cattle: A review focusing on the journal Theriogenology, the growth of the industry in North America, and personal reminisces. Theriogenology 2014; 81(1): 152-69.
[http://dx.doi.org/10.1016/j.theriogenology.2013.09.010] [PMID: 24274419]
[96]
Shima T, Sasaki Y, Itoh M, et al. Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J Reprod Immunol 2010; 85(2): 121-9.
[http://dx.doi.org/10.1016/j.jri.2010.02.006] [PMID: 20439117]
[97]
Brännström M, Giesecke L, Moore IC, van den Heuvel CJ, Robertson SA. Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol Reprod 1994; 50(5): 1161-7.
[http://dx.doi.org/10.1095/biolreprod50.5.1161] [PMID: 8025173]
[98]
Guleria I, Sayegh MH. Maternal acceptance of the fetus: True human tolerance. J Immunol 2007; 178(6): 3345-51.
[http://dx.doi.org/10.4049/jimmunol.178.6.3345] [PMID: 17339426]
[99]
Gaytán F, Morales C, García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE. Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod 1998; 59(2): 417-25.
[http://dx.doi.org/10.1095/biolreprod59.2.417] [PMID: 9687316]
[100]
Adashi EY. The potential relevance of cytokines to ovarian physiology: The emerging role of resident ovarian cells of the white blood cell series. Endocr Rev 1990; 11(3): 454-64.
[http://dx.doi.org/10.1210/edrv-11-3-454] [PMID: 2226351]
[101]
Goto J, Suganuma N, Takata K, et al. Morphological analyses of interleukin-8 effects on rat ovarian follicles at ovulation and luteinization in vivo. Cytokine 2002; 20(4): 168-73.
[http://dx.doi.org/10.1006/cyto.2002.1987] [PMID: 12543081]
[102]
Yasuda M, Shimizu S, Tokuyama S, Watanabe T, Kiuchi Y, Yamamoto T. A novel effect of polymorphonuclear leukocytes in the facilitation of angiogenesis. Life Sci 2000; 66(21): 2113-21.
[http://dx.doi.org/10.1016/S0024-3205(00)00537-3] [PMID: 10823350]
[103]
Turner EC, Hughes J, Wilson H, et al. Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction 2011; 141(6): 821-31.
[http://dx.doi.org/10.1530/REP-10-0327] [PMID: 21393340]
[104]
Oliveira LJ, Barreto RS, Perecin F, Mansouri-Attia N, Pereira FT, Meirelles FV. Modulation of maternal immune system during pregnancy in the cow. Reprod Domest Anim 2012; 47(Suppl. 4): 384-93.
[http://dx.doi.org/10.1111/j.1439-0531.2012.02102.x] [PMID: 22827396]
[105]
Ruocco MG, Chaouat G, Florez L, Bensussan A, Klatzmann D. Regulatory T-cells in pregnancy: Historical perspective, state of the art, and burning questions. Front Immunol 2014; 5: 389.
[http://dx.doi.org/10.3389/fimmu.2014.00389] [PMID: 25191324]
[106]
Lee SK, Kim JY, Lee M, Gilman-Sachs A, Kwak-Kim J. Th17 and regulatory T cells in women with recurrent pregnancy loss. Am J Reprod Immunol 2012; 67(4): 311-8.
[http://dx.doi.org/10.1111/j.1600-0897.2012.01116.x] [PMID: 22380579]
[107]
Voutilainen R, Tapanainen J, Chung BC, Matteson KJ, Miller WL. Hormonal regulation of P450scc (20,22-desmolase) and P450c17 (17 alpha-hydroxylase/17,20-lyase) in cultured human granulosa cells. J Clin Endocrinol Metab 1986; 63(1): 202-7.
[http://dx.doi.org/10.1210/jcem-63-1-202] [PMID: 3011839]
[108]
Jagger A, Shimojima Y, Goronzy JJ, Weyand CM. Regulatory T cells and the immune aging process: A mini-review. Gerontology 2014; 60(2): 130-7.
[http://dx.doi.org/10.1159/000355303] [PMID: 24296590]
[109]
Goto M. Inflammaging (inflammation + aging): A driving force for human aging based on an evolutionarily antagonistic pleiotropy theory? Biosci Trends 2008; 2(6): 218-30.
[PMID: 20103932]
[110]
Childs BG, Durik M, Baker DJ, van Deursen JM. Cellular senescence in aging and age-related disease: From mechanisms to therapy. Nat Med 2015; 21(12): 1424-35.
[http://dx.doi.org/10.1038/nm.4000] [PMID: 26646499]
[111]
Abrahams VM. Thirty years of reproductive immunology: An introduction. Am J Reprod Immunol 2010; 63(6): 411-2.
[http://dx.doi.org/10.1111/j.1600-0897.2010.00849.x] [PMID: 20565388]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy