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1 ISSCR San Francisco 24 June, 2005 Mechanisms of Pluripotency and Epigenesis in Human ESCs Roger A. Pedersen Department of Surgery Cambridge Institute for Medical Research University of Cambridge Cambridge Stem Cell Institute

2 Embryonic stem cells (ESCs) are derived from the ICM of blastocysts

3 Evaluation of hes cell epigenetic stability: genomic imprinting

4 Prevalent epigenetic instability in mouse ESC-derived fetuses Paternally expressed Igf2 U2af1-rs1 Maternally expressed H19 Igf2R Expression Altered Altered Altered Altered Methylation Imprint Altered Altered Altered Altered Dean et al., Devel. 125: 2273, 1998

5 Substantial epigenetic stability in hescs and their descendants Paternally expressed Igf2 KCNQNOT1 IPW Maternally expressed SLC22A18 NESP55/GNAS H19 Expression Stable Stable Stable Stable Stable Altered in one sub-line of H9 Methylation Imprint Maintained Maintained Maintained Maintained Not determined Maintained Rugg-Gunn, Ferguson-Smith and Pedersen, Nat. Genet.36: 585-7, 2005.

6 Pluripotency mechanisms differ between mouse and human ESCs FGF LIF ACT?? Smad 1 Ids BMPR 1/2 BMP BMP? hesc self-renewal mechanisms are still uncertain and could involve several growth factor families.

7 Nodal effect on hesc development Wild type hebs Day 10 of differentiation Nodal-expressing hebs Day 10 of differentiation Growth of EBs in CDM demonstrates morphogenetic effects of Nodal expression.

8 Nodal sustains expression of pluripotency marker Oct4 in EBs Oct-4 In situ hybridisation Oct 4 Immuno L1 L2 Wild Type D10 EB Nodal expressing D10 EB This reveals Nodal role in maintenance of pluripotency

9 Activin/Nodal signaling pathway /Nodal Ethier and Findlay, Reproduction, 2001

10 Nuclear location of Smads 2/3 in hescs grown on feeders Hoechst α Smad2 α Oct-4 α Oct-4 + Smad2 Smad3 Smad2 Hoechst α Smad3 α Oct-4 α Oct-4 + Smad3 Indicates activity of Nodal/Activin/TGFbeta signalling pathway

11 Expression of Activin and Nodal in hescs and feeders Activin Nodal TGFβ1 β2m Mouse Feeders + FGF -FGF hescs EBs Therefore, either mouse feeders or hescs themselves can be sources of pluripotency-inducing factors

12 Nodal and Activin independently sustain Tra-1-60 pluripotency marker expression on feeders Fraction of Tra-1-60 positive cells hescs Lefty-hESCs CerS-hESCs Nodal-hESCs Effects of Lefty or Cerberus (Nodal inhibitors) with increasing concentrations of follistatin (Activin inhibitor) confirm role of Activin/Nodal in hesc pluripotency.

13 Effect of SB inhibition of Activin/Nodal signaling on feeders 80 Fraction of Tra-1-60 positive cells days 10 days hescs hescs +SB 1μM hescs +SB 10μM hescs +SB 20μM Inhibition of Activin/Nodal receptor signalling confirms essential role in maintenance of hesc pluripotency.

14 CDM, a reduced complexity medium for hesc culture Chemically Defined Medium, Johansson and Wiles, % IMDM + 50% F12 NUT MIX 7 µg/ml insulin, 15 µg/ml transferrin, 450 µm monothioglycerol 5 mg/ml bovine serum albumin, Fraction V (Sigma)

15 Effects of Activin, FGF and their inhibitors (SB & SU5402) on hescs Fraction of Tra-1-60 positive cells Control Act 10 ng/ml + FGF 12 ng/ml FGF 12 ng/ml FGF 12 ng/ml + SB 10 µm FGF 12ng/ml + SU 10 µm Act 10 ng/ml Act 10 ng/ml + SB 10µM Act 10 ng/ml + SU 10 µm

16 Effects of other TGFb family members on Oct 4 expression in CDM 100% Oct-4 50% Oct-4 0% Oct Extent of Oct-4expression 0 Control Nodal 100ng/ml + FGF2 12 ng/ml Cripto 50 ng/ml TGFβ1 1 ng/ml BMP4 2ng/ml SB µM

17 Effects of Activin, FGF2 on Smad2 activity in hescs Activin A 10ng/ml Activin A + SU 10μM Activin A + 10ng/ml FGF2 Activin A + 20ng/ml FGF2 Activin A + 40ng/ml FGF2 FGF2 40 ng/ml Activin A + SB 10μM HePG2 Activin A 10ng/ml HePG2 Activin A 10ng/ml + SB 10μM PSmad2 Smad2 Therefore, maintenance of pluripotency marker expression in hescs correlates with extent of Smad2 activation

18 Longer term culture of hescs in CDM plus Activin/FGF hescs on feeders hescs in CDM + Activin + FGF 76% 80% Tra-1-60 pluripotency marker expression is maintained by Activin + FGF2 comparably to hescs on feeders

19 Pluripotency in human ESCs FGF FGFRs ACT Smad 2/3 Alk4/5/7 Smad 1 Ids BMPR 1/2 BMP hesc pluripotency is maintained by Activin/Nodal pathway, with FGF(s) acting as a competency factor.

20 Next Questions What are the mechanisms by which Activin/Nodal and FGFs maintain pluripotency? How long can hesc pluripotency, genetic normality and epigenetic stability be maintained in reduced complexity media with defined growth factors?

21 Conclusions Activin or Nodal, together with FGF2 are effective in sustaining pluripotency marker expression in hescs, in distinct contrast to mesc mechanisms. hescs have substantial epigenetic stability, contrasting with the relatively low epigeneitc stability of mescs. hescs provide novel insights into mechanisms uniquely involved in maintaining pluripotency and epigenetic stability at early stages of human development.

22 Acknowledgements Pedersen lab: Ludovic Vallier Peter Rugg-Gunn Kristie Pfendler (UCSF) Isabelle Bouhon Enrique Millan Joseph Smith Lucy Smithers (UCL) Morgan Alexander Kris Bowles Dan Reynolds Kamran Hussain Marie Corbel Ferguson-Smith lab: Neil Youngson Sylvia Kocialkowski Carol Edwards University of Sheffield: Peter Andrews British Heart Foundation

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