Telomeres and Genomic Instability In Preimplanation Embryos. David L. Keefe, M.D.
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1 Telomeres and Genomic Instability In Preimplanation Embryos David L. Keefe, M.D.
2 I. Global Genomic Instability, Including Aneuploidy, Mosaicism & Copy Number Variants, is Common In Preimplantation Embryos
3 Aneuploidy Contributes to Age-Related Infertility NYU Data 52% 50% 50.50% 47.70% 50% 35% 27% SART 18% Euploid 9% 2% < >42 Harton, Grifo, Munne et al. (2013) Fertil and Steril and unpublished data.
4
5 Mosaicism Definition- presence of two or more populations of cells with different genotypes in one individual, who has developed from a single fertilized egg. [1] Causes- mechanisms include chromosome non-disjunction, including correction of prior meiotic error, anaphase lag, and endoreplication. [2] Anaphase lag- is the most common way by which mosaicism arises in the preimplantation embryo. [2] [1] Stern, C. and K. Sekiguti Bio. Zentr. 51, [2]Fitzgerald, P. H.; Donald, R. A.; Kirk, R. L (1979). Clinical genetics. 15 (1): 89
6 Is Mosaicism Real? How Reliable & Accurate is NGS? Retrospective study of embryos that had undergone PGS by NGS Reprogenetics) from 2/15-1/17. Thawed, expanded, re-biopsied, repeated NGS using same WGA, Veriseq, MiSeq, but in our own laboratory Blastocysts w/ diagnosis of mosaic, aneuploid or euploid Whole Genome Amplification (WGA) by Sureplex Veriseq DNA library prep MiSeq sequencing to assess chromosomal copy number BlueFuse Multi software Aneuploidy- >80% change in chromosome copy number Mosaicism- examined varying thresholds from 20-80% (per PGDIS); also looked at 30% and 40% thresholds Nidhee et al, ASRM 2017
7 How Reliable & Accurate is NGS? 129 samples from 32 blastocysts from 17 patients 18 mosaic, 4 aneuploid and 10 euploid Concordance for aneuploidy- 97% (62/64 samples) Concordance b/w ICM/TE for aneuploidy- 100% 2 non-concordant samples between TE biopsies, but both showed either aneuploidy for another chromosome or complex mosaicism with more than 3 chromosomes mosaic.. Nidhee et al, ASRM 2017
8 How Reliable & Accurate is NGS? Mosaic chromosome not identified consistently in repeat biopsy specimens, regardless of diagnostic criteria used to call mosaicism Concordance for mosaicism between clinical and experimental biopsies not affected by varying diagnostic threshold for mosaicism Concordance for mosaicism not different between TE and ICM Number of samples with additional mosaic chromosomes (a chromosome in addition to the chromosome previously diagnosed to be mosaic) significantly varied between the different diagnostic thresholds (p <0.001). Number of cells included in the biopsy did not affect concordance for mosaicism across all diagnostic threshold levels Nidhee et al, ASRM 2017
9 Aneuploid Euploid Euploid embryo
10 Aneuploid Euploid Aneuploid embryo
11 Aneuploid Euploid Mosaic embryo
12 Summary and Conclusions- Mosaicism & Reliability PGS by NGS PGS previously thought to provide a binary output- normal vs. abnormal With increased sensitivity associated with acgh and NGS, PGS now detects more subtle abnormalities PGS w/ NGS provides a continuous output, similar to glucose tolerance test for diagnosis of diabetes mellitus More studies needed to optimize clinical utility of PGS
13 Anaphase lag- delayed movement during anaphase, where one homologous chromosome in meiosis or one chromatid in mitosis fails to connect to the spindle apparatus, or is tardily drawn to its pole and fails to be included in the reforming nucleus. Chromosome forms a micronucleus in the cytoplasm and is lost from the cell. [1] The lagging chromosome is not incorporated into the nucleus of one of the daughter cells, resulting in one normal daughter cell and one with monosomy. [2] Anaphase lag can also cause a rescue of the daughter cell if the cell was originally trisomy. [1] [1] Gardner, R.J.M; Sutherland, Grant R. (2004). Chromosome Abnormalities and Genetic Counseling (3rd ed.). NY: Oxford Press. [2] Jump up^ "Human Molecular Genetics". Archived from the original on June 29, 2007.
14 Anaphase Lag & Mosaicism
15 II. Telomeres & Genomic Instability in Preimplantation Embryos
16 Telomere- Structure Tandem repeats (TTAGGG) 6 proteins in a complex known as Shelterin. Fold single stranded end of chromosome into a t- loop to avoid DNA damage response. Loss of telomere leads to apoptosis or senescence.
17 Telomeres Protect Against DNA Damage Response
18 Telomeres Shorten With Age Njajou et al. PNAS, 2007
19 Telomerase activity Telomerase Activity Is Very Low During Late Oogenesis/Early Embryo Development egg(d. 0) zygote (d. 1) 2 cell (d. 2) morula (d. 3) bastocyst (d. 4) Wright et al, Develop Genetics, 1996
20 Telomere Attrition in Mice Phenocopies Reproductive Aging in Women Observation Production Line (Henderson and Edwards, 1968) Decreased Chiasmata- (Hassold et al, 1996) Spindle abnormalities- (Battaglia et al,1997) Low levels mtdna deletions & ROS - (Keefe et al, 1995) Increased embryo fragmentation & apoptosis (Juriscova et al, 2003) Keefe & Liu, 2009 Explained by Telomere Theory
21 Reproductive Function in Patient With Telomeropathy Unaffected Patient (29-31) DKC (30 years old) Anti-Mullerian Hormone Stimulation Dosage 200 IU 600IU Stimulation Duration Oocytes Retrieved % Fertilized 90% 40% % of Euploid embryos 50% 14% Robinson et al, unpublished
22 Short Telomeres in Embryos From Telomereopathy (DKC) Patient N.S. P.05 P.05 Robinson et al, unpublished
23 Alternative Lengthening of Telomeres- ALT
24 2007
25 Telomeres Are Short in Oocytes and Elongate in Embryos- Even Parthenotes
26 Telomere Elongation- Even in Telomerase Null Mice
27 Telomere Elongation- Associated with Telomere-Sister Chromatid Exchange
28 DNA Double Strand Break Repair- Rad 50, Bloom, Werner- During Cleavage Stage
29 Double Strand Break Repair Proteins- Preferentially Associated with Telomeres
30 Telomere Lengthen Across Preimplantation Development in Human Embryos P=.03 P=.0002 N.S. P =.03 Text Robinson et al, unpublished
31 What About Women? Telomeres Lengthen in Parthenotes Following Activation N.S. P =.019 P =.003 N= 37 N= 21 N= 16 N= 32 Robinson et al, unpublished
32 III. What Causes Alternative Lengthening of Telomeres in Preimplantation Embryos?
33 Flies Elongate Telomeres Via Retrotransposition
34
35 Line 1- Long Interspersed Element Active retrotransposon- maintains reverse transcriptase & endonuclease activity Comprises 17% of human genome With other, inactive transposable elements, e.g. Alu & Sine, comprise 40% of human genome These parasites infected our ancestral genome billions of years ago Held in check by methylation of CpG islands in 5 promoter region and by histone methylation Cytosine demethylation during oogenesis & early embryo development resets the epigenetic clock Cytosine demethylation activates Line 1 Activation of Line 1 implicated in fetal oocyte attrition in mice
36 Cytosine Demethylation During Gametogenesis & Early Development
37 Do Mammals Mobilize Retrotransposons To Elongate Telomeres During Early Development? Telomere RNA (TERRA) Expressed (Wang) ALT in human embryos & parthenotes (Robinson) Telomere elongation inhibited by AZT (Navarro) ORF2 expressed in embryos? (Bourroul) Methylome clock advanced in individual human oocytes? (Wang, Charmani) Retrotransposon capture (RC) seq to compare TE architecture in euploid vs. aneupoid human embryos; persistence of LINE1 message in abnormal blasts? (Maxwell)
38 Summary & Conclusions Genomic instability is common in preimplantation embryos Mitotic as well as meiotic errors- mosaicism, copy number variants Telomeres are essential for genomic stability DNA recombination-based telomere elongation, which resembles retrotransposon activation, may contribute to global genomic instability during preimplantation embryo development
39 Acknowledgements Laboratory for Human Reproduction David L. Keefe Fang Helen Wang Ricardo Pimentel (Univ. Fed. De Goias) Libing Wang (UCLA) Lan Wang (Tongji Med. College) Elisa Atamian (Boston Univ.) Jason Kofinas (Kofinas Ferility) Dani Antunes (NYU FC) Molly Kumar (University of Sydney) Lin Liu (Univ. Nankai) Nidhee Sachdev Paula Navarro (USP-RP, Brazil) NYU Fertility Center Yael Kramer David McCulloh Jamie Grifo & Embryology Staff New York Stem Cell Foundation Deter Egli Funding March of Dimes Stanley Kaplan Research Endowment
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