Cellular Therapies December 9, 2013
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1 Cellular Therapies December 9, 2013 Scott C. Baraban, Ph.D. University of California, San Francisco American Epilepsy Society Annual Meeting
2 Disclosure Neurona Therapeutics Co-founder BioCrea - Consultant Dravet Syndrome Foundation SAB Grant Support NIH (NINDS), C.U.R.E., DSF, AES, CIRM American Epilepsy Society 2013 Annual Meeting
3 Learning Objectives Understand current cell therapy approaches to control intractable seizures Discuss potential limitations in moving these approaches toward the clinic American Epilepsy Society 2013 Annual Meeting
4 Problem: epilepsy is a network phenomena increased neuronal bursting and synchronization are a hallmark of seizures Worrell G A et al. Brain 2004 Morgan RJ, Soltesz I. Proc Natl Acad Sci 2008
5 Inhibition may be the best way to constrain an epileptic network Evidence of an inhibitory restraint of seizure activity in humans. Schevon et al. Nat Comm 2012 How inhibition influences seizure propagation. Trevelyan AJ, Schevon CA. Neuropharmacology 2013
6 How do we increase inhibition? GABA mimetic drugs Modulation of postsynaptic GABA receptors Block GABA re-uptake New GABA interneurons?
7 A strategy for cell therapy 1. Identify epileptic zone 2. Cell transplantation 3. Cell integration and seizure control Adapted from Parent & Murphy News & Views; Nature Neuroscience 2013
8 Modulation of experimentally induced epilepsy by intracerebral grafts of fetal GABAergic neurons Fine A, Meldrum BS. Neuropsychologia 1990
9 Benefits and risks of intranigral transplantation of GABAproducing cells subsequent to the establishment of kindlinginduced seizures Nolte MW, Löscher W, Herden C, Freed WJ, Gernert M. Neurobiol Dis. 2008
10 Why earlier approaches did not work? Failure of transplanted cells to integrate Mixed populations of transplanted cells Mechanism of action?? Not tested in appropriate animal model
11 A path to the clinic: preclinical studies Obtain proof-of-principle data in an animal model of epilepsy Generation of inhibitory interneurons Functional integration following transplantation Disease-modifying activity (DMA) against spontaneous seizures and related co-morbidities American Epilepsy Society 2013 Annual Meeting
12 How to make an interneuron for cell therapy E13.5 mouse Source: embryonic medial ganglionic eminence (MGE) neuron expressing GABA migration in host brain mature firing properties integration in host circuitry
13 MGE cells migrate widely in host brain P2 transplant (up to 5 mm) P60 transplant (up to 2 mm) cortex, hippocampus, amygdala
14 MGE cells enhance inhibition in host brain fetal MGE progenitor cells IPSC onto host pyramidal cortex and hippocampus
15 Optogenetic manipulation of MGE-derived interneurons following transplantation Robert F. Hunt III
16 MGE cells in a genetic form of epilepsy Kv1.1 null mice P2 MGE transplant 96% seizure reduction Baraban SC, Southwell DG, Estrada RC, Jones DL, Sebe JY, Alfaro-Cervello C, Garcia-Verdugo JM, Rubenstein JL, Alvarez-Buylla A. Proc. Natl. Acad. Sci. USA 2009
17 MGE cells in an acquired form of epilepsy pilocarpine model of TLE adult MGE transplant 92% seizure reduction Hunt RF, Girskis KM, Rubenstein JL, Alvarez-Buylla A, Baraban SC. Nat. Neuroscience 2013
18 How to make a neuron: induced neural cells defined transcription factors direct cell fate Yang N, Ng YH, Pang ZP, Sudhof TC, Wernig M. Cell Stem Cell 2011
19 Features of an ideal human MGE cell line GABA interneuron specificity PV, SOM, NPY Robust migration Functional integration Safety Efficacy American Epilepsy Society 2013 Annual Meeting
20 Some currently available human stem cell lines 1. Sox1-expressing embryonic stem cells (ESC) 2. Nkx2.1-expressing embryonic stem cells (ESC) 3. induced pluripotent stem cells (ipsc) from Dravet patients Maisano et al. J Neurosci 2012; Liu et al. Nat Biotechnol 2013; Maroof et al. Cell Stem Cell 2013; Nicholas et al. 2013; Liu et al. Ann Neurol 2013; Jiao et al. Hum Mol Genet 2013; Shirasaka et al. Mol Brain 2013
21 Human SC-derived interneurons in vitro Kevin Ess Arturo Alvarez-Buylla, John Rubenstein Arnold Kriegstein GABA / b-tubulin III Stewart Anderson Lorenz Studer Lori Isom Jack Parent Su-Chun Zhang
22 Potential problems: Slow differentiation NKX2.1::GFP human ES cells FACS sorted and transplanted into neonatal cortex 6 wk - 3 mo. post-transplantation: undifferentiated appearance... often tipped by growth cones Maroof AM, Keros S, Tyson JA, Ying SW, Ganat YM, Merkle FT, Liu B, Goulburn A, Stanley EG, Elefanty AG, Widmer HR, Eggan K, Goldstein PA, Anderson SA, Studer L. Cell Stem Cell 2013
23 Potential problems: Slow functional maturation NKX2.1::GFP human ES cells FACS sorted/neonatal cortex 7 months post-transplant Nicholas CR, Chen J, Tang Y, Southwell DG, Chalmers N, Vogt D, Arnold CM, Chen YJ, Stanley EG, Elefanty AG, Sasai Y, Alvarez-Buylla A, Rubenstein JL, Kriegstein AR. Cell Stem Cell 2013
24 Potential problems: Teratocarcinoma undifferentiated hes cells hippocampus transplant Sox1:GFP::Ubi:RFP cells Germain ND, Hartman NW, Cai C, Becker S, Naegele J, Grabel LB. Cell Transplant 2012
25 How do we address these problems? Learn more about the properties of fetal human MGE cells Improve methods or techniques for generating hmge cells Develop and characterize more appropriate animal models for evaluation of human MGE cells
26 Properties of human MGE cells Subcortical origins of human and monkey neocortical interneurons. Ma et al. Nat Neuroscience 2013 Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Hansen et al. Nat Neuroscience 2013
27 Cerebral organoids as MGE donors? Cerebral organoids model human brain development and microcephaly. Lancaster et al. Nature 2013 Self-organization of axial polarity, inside-out layer pattern, and species progenitor dynamics in human ES cell-derived neocortex. Kadoshima et al. Proc Natl Acad Sci USA 2013
![Human stem cell therapies that are showing some promise (but not epilepsy, yet) Neural stem cell engraftment and myelination in the human brain. [leukodystrophy] Gupta et al.](/docs-images/85/91363547/images/28-1.jpg "Sci Transl Med 2012 Central nervous system stem cell transplantation for children with neuronal ceroid lipofuscinosis. J Neursurg Pediatr.")
28 Human stem cell therapies that are showing some promise (but not epilepsy, yet) Neural stem cell engraftment and myelination in the human brain. [leukodystrophy] Gupta et al. Sci Transl Med 2012 Central nervous system stem cell transplantation for children with neuronal ceroid lipofuscinosis. J Neursurg Pediatr HuCNS-SC oligodendrocytes, neurons and astrocytes
29 A path to the epilepsy clinic Obtain IND enabling data with a human MGE cell line Disease Modifying Activity (DMA) in at least one animal model of epilepsy Safety and dosing information Cryopreservation Device for delivery of human MGE cells American Epilepsy Society 2013 Annual Meeting
30 (Future) Impact on Clinical Care and Practice Tissue grafts transiently suppress evoked seizures
31 (Future) Impact on Clinical Care and Practice Tissue grafts transiently suppress evoked seizures Mouse MGE cells suppress spontaneous seizures & reverse comorbidities
32 (Future) Impact on Clinical Care and Practice Human MGE cells are safe and suppress seizures in patients Tissue grafts transiently suppress evoked seizures Mouse MGE cells suppress spontaneous seizures & reverse comorbidities
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