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Perspectives of Stem Cells
Henning UlrichEditor
Perspectivesof Stem Cells
From Tools for StudyingMechanisms of NeuronalDifferentiation towards Therapy
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EditorProf. Henning UlrichUniversidade de Sao PauloInstituto de QuimicaDepartamento de BioquimicaAv. Prof. Lineu Prestes 748Sao [email protected]
ISBN 978-90-481-3374-1 e-ISBN 978-90-481-3375-8DOI 10.1007/978-90-481-3375-8Springer Dordrecht Heidelberg London New York
Library of Congress Control Number: 2009940404
© Springer Science+Business Media B.V. 2010No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or byany means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without writtenpermission from the Publisher, with the exception of any material supplied specifically for the purpose ofbeing entered and executed on a computer system, for exclusive use by the purchaser of the work.
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Preface
Stem cells are fascinating cell types. They can replicate themselves forever whileretaining the potential to generate progeny with specific functions. Because of thesespecial properties, stem cells have been subjects of intensive investigation, fromunderstanding basic mechanisms underlying tissue generation, to modeling humandiseases, to application for cell replacement therapy. Stem cells come in differentforms. For example, mouse embryonic stem cells can general all cell types in a body,either in a dish or when put back into mouse embryos. On the other hand, neuralstem cells in the adult brain generate neurons and glia cells that contribute to thebrain’s plasticity. Rapid progress has been made in the stem cell field with discover-ies published in a record speed. A quick Pubmed search has returned 2789 hits for“embryonic stem cells” and 815 hits for “adult neural stem cells/neurogenesis” in theyear 2008 alone. It remains a taunting task for all who are interested in stem cells tokeep up with rapidly accumulating literatures. The “Perspectives of Stem Cells” by atruly international team of experts provides a timely and invaluable highlight of thestem cell field gearing toward future therapeutic applications in the nervous system.
Stem cells with neural potentials have attracted a lot of attention because of theirpromise for cell replacement therapy, ranging from degenerative neurological disor-ders to spinal cord injuries. Before such potentials to be realized, however, we needto understand the basic biology of these stem cells. For example, understanding howstem cell behaviors are controlled by intrinsic and extrinsic factors will help to directstem cells into a specific fate while avoiding undesired tumorigenesis. Equally impor-tant, we need to understand adult nervous system milieu where substitute neuronsneed to integrate into proper circuitry for maximal recovery. In this regard, the recentdiscovery of functional neurogenesis in discrete regions of the adult mammalianbrain, including humans, has a major impact on regenerative medicine. Not onlythere exist residual adult neural stem cells as endogenous cellular sources for neu-rogenesis, the adult nervous system itself exhibits surprising plasticity. They provideproper signals to support normal neurogenesis and, furthermore, additional signalsupon injuries to activate neural stem cells and guide their neuronal progeny to theright location. The dogma, “In the adult centers, the nerve paths are something fixed,ended, and immutable. Everything may die, nothing may be regenerated”, is now longgone.
The Prospective covers a broad spectrum of a fast evolving field of stem cells:from different model systems and stem cell types, to their cell biology and molecu-lar signaling mechanisms; from overview of protocols for directed neuronal subtypedifferentiation from embryonic stem cells, and even the latest induced pluripotent
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stem cells, to specific considerations for the therapeutic application. The historicalview of neurogenesis since the time of Cajal was a delight retreat; the discussion ofretrotransposons in generating neuronal diversity through neurogenesis was fascinat-ing. The Prospective provides a much needed overview of the state of the art in thefield and a rich resource of updated information. More importantly, it sets up a stagefor flourishing of new ideas in stem cell biology and for fostering novel therapeuticapplications in the nervous system for years to come.
Clarksville, Maryland Hongjun SongAugust 2009
Editor Preface
The field of stem cell biology is geared towards translation into clinical practicethrough in vitro tissue production and regeneration therapy. The discovery of neu-rogenesis in selected areas of the adult brain has revolutionized neuroscience. Thisdiscovery has overturned the central assumption that no new neurons were origi-nated in the brain after birth, and provided the basis for understanding the molecularmechanisms of neural differentiation. Several in vitro models have been developedto investigate signalling pathway of neurogenesis regulation and cell fate specifica-tion. Massive propagation of embryonic cells into just the right type of phenotypeof a neural progenitor cell or strategies for mobilizing endogenous neural stem orprogenitor cells provide replacement therapies for brain injury resulting from strokeor neurodegenerative diseases. Such strategies are getting more important, since thedevelopment of ex vivo cultures of stem cells allows collection of multipotent cellsfrom patients, their differentiation and transplantation into diseased areas.
This book includes a chapter on mechanisms of neural induction in early embryosas well as a detailed discussion of changes in paradigms in view of the discov-ery of adult neurogenesis. Neuronal differentiation is detailed using the olfactoryepithelium, one of the tissues bearing neurogenesis along life. In addition to chapterson therapeutic applicability of embryonic, very small-embryonic like, mesenchymalstem and neural progenitor cells, this book covers signalling mechanisms guidinginduction to differentiation and selective achievement of specific phenotypes. Celldiversification of the neuronal system is explained using the example of neural crestcell differentiation. Alterations in genetic material, such as loss of chromosomesand retrotransposition, are discussed as possible mechanisms for cell diversification.Furthermore, fundamental aspects of stem cell biology and neurogenesis, such as theimportance of proliferation induction, programmed cell death, as well as the func-tion of glia in differentiation of stem cells and development of neuronal circuits, arealso highlighted. The participation of cytoskeletal elements in cell polarization as pre-requisites of asymmetric division and differentiation induction is discussed. Furthertopics include the analysis of extracellular signals, such as neurotrophic factors andneurotransmitters, their receptor molecules and the propagation of these signals byintracellular signal transduction leading to activation of selective gene expression dur-ing differentiation. Rhythmic gene expression for activation and inhibition of Notchsignalling is discussed as a mechanism for regulating the progress of neurogenesis. Invitro cultures of embryonic, mesenchymal and neural stem cells as well as mobiliza-tion of endogenous stem and precursor cells for brain repair and replacement therapyin neurological disorders are important issues of this book.
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Each chapter provides an invaluable resource for information on the most currentadvances in the field and possible therapeutic applications, with discussions of con-troversial issues and areas of emerging importance. By providing an up-to-date andcritical view of the state of Science, we hope that this book shall be a base for excit-ing scientific ideas regarding functions and therapeutic applications of stem cells inthe adult brain. The book is directed to neuroscientists, physicians, students and allwho are engaged and interested in the exciting and rapidly expanding field of modernneuroscience and stem cell biology.
São Paulo Henning UlrichJune 2009
Contents
1 Neural Induction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1Karla Loureiro Almeida, José Abreu, and C. Y. Irene Yan
2 Neurogenesis: A Change of Paradigms . . . . . . . . . . . . . . . . 11Luiz E. Mello and Beatriz M. Longo
3 Neurogenesis in the Olfactory Epithelium . . . . . . . . . . . . . . . 35Bettina Malnic and Lucia Armelin-Correa
4 Cell Diversification During Neural Crest Ontogeny:The Neural Crest Stem Cells . . . . . . . . . . . . . . . . . . . . . . 47Elisabeth Dupin, Giordano W. Calloni, and Nicole M. LeDouarin
5 Intermediate Filament Expression in Mouse EmbryonicStem Cells and Early Embryos . . . . . . . . . . . . . . . . . . . . . 59Zhigang Xue, Vivaldo Moura-Neto, Araksya Izmiryan,Sheila Cristina de Souza Martins, Jean Christophe Larcher,Denise Paulin, and Zhenlin Li
6 Aneuploidy in Embryonic Stem Cells . . . . . . . . . . . . . . . . . 73Rafaela C. Sartore, Priscila B. Campos,Michael J. McConnell, and Stevens K. Rehen
7 Retrotransposition and Neuronal Diversity . . . . . . . . . . . . . . 87Maria C. N. Marchetto, Fred H. Gage, and Alysson R. Muotri
8 Directing Differentiation of Embryonic Stem Cellsinto Distinct Neuronal Subtypes . . . . . . . . . . . . . . . . . . . . 97Noelle Ammon, Nathaniel Hartman, and Laura Grabel
9 Neurotransmitters as Main Players in the NeuralDifferentiation and Fate Determination Game . . . . . . . . . . . . 115Katia K. Yuahasi, Katia N. Gomes, Marcelo Campos, ArthurA. Nery, Ariane Nunes-Alves, Cleber A. Trujillo, and Henning Ulrich
10 Rhythmic Expression of Notch Signaling in NeuralProgenitor Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135Hiromi Shimojo, Toshiyuki Ohtsuka, and Ryoichiro Kageyama
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11 Neuron-Astroglial Interactions in Cell Fate Commitmentin the Central Nervous System . . . . . . . . . . . . . . . . . . . . . 145Joice Stipursky, Tânia Cristina Leite de Sampaio e Spohr,Luciana Ferreira Romão, and Flávia Carvalho Alcantara Gomes
12 The Origin of Microglia and the Development of the Brain . . . . . 171Flavia R. S. Lima, Anna Carolina C. da Fonseca,Giselle P. Faria, Luiz Gustavo F. Dubois, Tércia R. Alves,Jane Faria, and Vivaldo Moura Neto
13 Tissue Biology of Proliferation and Cell Death AmongRetinal Progenitor Cells . . . . . . . . . . . . . . . . . . . . . . . . 191Rafael Linden, Rodrigo A.P. Martins, Mariana S. Silveira,Helena L. Borges, Alfred Sholl-Franco, LucianneFragel-Madeira, and Ana Carolina Dudenhoeffer-Carneiro
14 Potential Application of Very Small Embryonic Like(VSEL) Stem Cells in Neural Regeneration . . . . . . . . . . . . . . 231Mariusz Z. Ratajczak, Ewa Zuba-Surma, Magda Kucia,Przemyslaw Nowacki, and Bogdan Machalinski
15 Embryonic Stem Cell Transplantation for the Treatmentof Parkinson’s Disease . . . . . . . . . . . . . . . . . . . . . . . . . 245Asuka Morizane and Jun Takahashi
16 Functional Multipotency of Neural Stem Cellsand Its Therapeutic Implications . . . . . . . . . . . . . . . . . . . 255Yang D. Teng, Serdar Kabatas, Jianxue Li,Dustin R. Wakeman, Evan Y. Snyder, and Richard L. Sidman
17 Dual Roles of Mesenchymal Stem Cells in Spinal CordInjury: Cell Replacement Therapy and as a Model Systemto Understand Axonal Repair . . . . . . . . . . . . . . . . . . . . . 271Cecile King, Shyam Patel, Treena Livingston Arinzeh,and Pranela Rameshwar
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285
Contributors
José Abreu Cellular and Developmental Biology Program, Institute of BiomedicalSciences, Universidade Federal do Rio de Janeiro, Centro de Ciências da Saúde –bloco F, Cidade Universitária, Rio de Janeiro, RJ 21949-590, Brazil,[email protected]
Karla Loureiro Almeida Departamento de Morfologia, Centro de Ciências daSaúde, Universidade Federal do Espírito Santo - Vitória/ES - Brazil,[email protected]
Ariane Nunes-Alves Departamento de Bioquímica, Instituto de Química,Universidade de São Paulo, São Paulo, Brazil, [email protected]
Tércia R. Alves Programa de Anatomia, Instituto de Ciências Biomédicas,Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil,[email protected]
Noelle Ammon Hall-Atwater Laboratories, Biology Department, WesleyanUniversity, Middletown, CT, USA, [email protected]
Lucia Armelin-Correa Departamento de Bioquímica, Instituto de Química,Universidade de São Paulo, São Paulo, Brazil, [email protected]
Helena L. Borges Instituto de Ciências Biomédicas, Universidade Federal do Riode Janeiro, Cidade Universitaria, Rio de Janeiro, Brazil, [email protected]
Giordano W. Calloni CNRS UPR2197 Laboratoire Développement, Evolution etPlasticité du Système Nerveux, Institut de Neurobiologie Alfred Fessard, 91198Gif-sur-Yvette, France; Departamento de Biologia Celular, Embriologia e Genética,Centro de Ciências Biológicas, Universidade Federal de Santa Catarina,Florianópolis, Brazil, [email protected]
Priscila B. Campos Instituto de Ciências Biomédicas, Universidade Federal do Riode Janeiro, Rio de Janeiro, Brazil, [email protected]
Marcelo Campos Departamento de Bioquímica, Instituto de Química,Universidade de São Paulo, São Paulo, Brazil, [email protected]
Anna Carolina C. da Fonseca Programa de Anatomia, Instituto de CiênciasBiomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil,[email protected]
Luiz Gustavo F. Dubois Programa de Anatomia, Instituto de Ciências Biomédicas,Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, [email protected]
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xii Contributors
Ana Carolina Dudenhoeffer-Carneiro Instituto de Biofísica, UniversidadeFederal do Rio de Janeiro, Cidade Universitaria, Rio de Janeiro, Brazil,[email protected]
Elisabeth Dupin CNRS UPR2197 Laboratoire Développement, Evolution etPlasticité du Système Nerveux, Institut de Neurobiologie Alfred Fessard, 91198Gif-sur-Yvette, France, [email protected]
Giselle P. Faria Programa de Anatomia, Instituto de Ciências Biomédicas,Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil,[email protected]
Jane Faria Programa de Anatomia, Instituto de Ciências Biomédicas, UniversidadeFederal do Rio de Janeiro, Rio de Janeiro, Brazil, [email protected]
Lucianne Fragel-Madeira Instituto de Biofísica, Universidade Federal do Rio deJaneiro, Cidade Universitaria, Rio de Janeiro, Brazil, [email protected]
Fred H. Gage Laboratory of Genetics, The Salk Institute for Biological Studies, LaJolla, CA, USA, [email protected]
Katia N. Gomes Departamento de Bioquímica, Instituto de Química, Universidadede São Paulo, São Paulo, Brazil, [email protected]
Flávia Carvalho Alcantara Gomes Laboratório de Neurobiologia Celular,Programa de Biologia Celular e do Desenvolvimento, Instituto de CiênciasBiomédicas, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro,Rio de Janeiro, Brazil, [email protected]
Laura Grabel Hall-Atwater Laboratories, Biology Department, WesleyanUniversity, Middletown, CT, USA, [email protected]
Nathaniel Hartman Hall-Atwater Laboratories, Biology Department, WesleyanUniversity, Middletown, CT, USA, [email protected]
Araksya Izmiryan UPMC Univ Paris 6, UMR 7079, Paris, France,[email protected]
Serdar Kabatas Department of Neurosurgery, Baskent University IstanbulHospital, Istanbul, Turkey, [email protected]
Ryoichiro Kageyama Institute for Virus Research, Kyoto University, Kyoto, Japan;Japan Science and Technology Agency, CREST, Kyoto, Japan,[email protected]
Cecile King UMDNJ-New Jersey Medical School, Department of Medicine,Newark, NJ, USA, [email protected]
Magda Kucia Stem Cell Institute at James Graham Brown Cancer Center,University of Louisville, Louisville, KY, USA, [email protected]
Jean Christophe Larcher Laboratoire de Biologie du Développement, Paris,France, [email protected]
Nicole M. Le Douarin CNRS UPR2197 Laboratoire Développement, Evolution etPlasticité du Système Nerveux, Institut de Neurobiologie Alfred Fessard, 91198Gif-sur-Yvette, France, [email protected]
Contributors xiii
Jianxue Li Department of Neurology, Beth Israel Deaconess Medical Center,Harvard Medical School, Boston, MA, USA, [email protected]
Zhenlin Li UPMC Univ Paris 6, UMR 7079, Paris, France, [email protected]
Flavia R.S. Lima Programa de Anatomia, Instituto de Ciências Biomédicas,Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, [email protected]
Rafael Linden Instituto de Biofísica, Universidade Federal do Rio de Janeiro,Cidade Universitaria, Rio de Janeiro, Brazil, [email protected]
Treena Livingston Arinzeh New Jersey Institute of Technology, Department ofBiomedical Engineering, Newark, NJ, USA, [email protected]
Beatriz M. Longo Departamento de Fisiologia, Universidade Federal de São Paulo,São Paulo, Brazil, [email protected]
Bogdan Machalinski Department of Physiopathology Pomeranian MedicalUniversity, Szczecin, Poland, [email protected]
Bettina Malnic Departamento de Bioquímica, Instituto de Química, Universidadede São Paulo, São Paulo, Brazil, [email protected]
Maria C. N. Marchetto Laboratory of Genetics, The Salk Institute for BiologicalStudies, La Jolla, CA, USA, [email protected]
Sheila Cristina de Souza Martins Instituto de Ciências Biomédicas-UniversidadeFederal de Rio de Janeiro, Rio de Janeiro, Brazil, [email protected]
Rodrigo A.P. Martins Instituto de Biofísica, Universidade Federal do Rio deJaneiro, Cidade Universitaria, Rio de Janeiro, Brazil, [email protected]
Michael J. McConnell Crick-Jacobs Center for Theoretical and ComputationalBiology, Salk Institute for Biological Studies, La Jolla, California, USA,[email protected]
Luiz E. Mello Departamento de Fisiologia, Universidade Federal de São Paulo, SãoPaulo, Brazil, [email protected]
Asuka Morizane Department of Biological Repair, Institute for Frontier MedicalSciences, Kyoto University, Kyoto, Japan, [email protected]
Vivaldo Moura-Neto Instituto de Ciências Biomédicas-Universidade Federal deRio de Janeiro, Rio de Janeiro, Brazil, [email protected]
Alysson Muotri University of California at San Diego, School of Medicine,Department of Pediatrics/Rady Children’s Hospital San Diego and Department ofPediatrics/Cellular and Molecular Medicine, La Jolla, CA, USA, [email protected]
Arthur A. Nery Departamento de Bioquímica, Instituto de Química, Universidadede São Paulo, São Paulo, Brazil, [email protected]
Przemyslaw Nowacki Department of Physiopathology Pomeranian MedicalUniversity, Szczecin, Poland, [email protected]
Toshiyuki Ohtsuka Institute for Virus Research, Kyoto University, Kyoto, Japan;Japan Science and Technology Agency, CREST, Kyoto, Japan,[email protected]
xiv Contributors
Shyam Patel UMDNJ-New Jersey Medical School, Department of Medicine,Newark, NJ, USA, [email protected]
Denise Paulin UPMC Univ Paris 6, UMR 7079, Paris, France,[email protected]
Pranela Rameshwar UMDNJ-New Jersey Medical School, Department ofMedicine, Newark, NJ, USA, [email protected]
Mariusz Z. Ratajczak Stem Cell Institute at James Graham Brown Cancer Center,University of Louisville, Louisville, KY, USA; Department of PhysiopathologyPomeranian Medical University, Szczecin, Poland, [email protected]
Stevens K. Rehen Instituto de Ciências Biomédicas, Universidade Federal do Riode Janeiro, Rio de Janeiro, Brazil, [email protected]
Luciana Ferreira Romão Laboratório de Neurobiologia Celular, Programa deBiologia Celular e do Desenvolvimento, Instituto de Ciências Biomédicas, Centro deCiências da Saúde, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil,[email protected]
Rafaela C. Sartore Instituto de Ciências Biomédicas, Universidade Federal do Riode Janeiro, Rio de Janeiro, Brazil, [email protected]
Hiromi Shimojo Institute for Virus Research, Kyoto University, Kyoto, Japan;Japan Science and Technology Agency, CREST, Kyoto, Japan,[email protected]
Alfred Sholl-Franco Instituto de Biofísica, Universidade Federal do Rio deJaneiro, Cidade Universitaria, Rio de Janeiro, Brazil, [email protected]
Richard L. Sidman Department of Neurology, Beth Israel Deaconess MedicalCenter, Harvard Medical School, Boston, MA, USA,[email protected]
Mariana S. Silveira Instituto de Biofísica, Universidade Federal do Rio de Janeiro,Cidade Universitaria, Rio de Janeiro, Brazil, [email protected]
Evan Y. Snyder Stem Cell and Regeneration Program, The Burnham Institute, LaJolla, CA, USA, [email protected]
Tânia Cristina Leite de Sampaio e Spohr Laboratório de Neurobiologia Celular,Programa de Biologia Celular e do Desenvolvimento, Instituto de CiênciasBiomédicas, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro,Rio de Janeiro, Brazil, [email protected]
Joice Stipursky Laboratório de Neurobiologia Celular, Programa de BiologiaCelular e do Desenvolvimento, Instituto de Ciências Biomédicas, Centro de Ciênciasda Saúde, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil,[email protected]
Jun Takahashi Department of Biological Repair, Institute for Frontier MedicalSciences, Kyoto University, Kyoto, Japan, [email protected]
Contributors xv
C.Y. Irene Yan Department of Cell and Developmental Biology, Institute ofBiomedical Sciences, Universidade de São Paulo, Av. Prof Lineu Prestes 1524, SãoPaulo, SP 05508-900, Brazil, [email protected]
Yang D. Teng Department of Neurosurgery, Harvard Medical School, Brigham andWomen’s Hospital, and Children’s Hospital Boston, Boston, MA, USA; Departmentof Physical Medicine and Rehabilitation, Harvard Medical School, SpauldingRehabilitation Hospital, Boston, MA, USA; Division of SCI Research, VeteransAffairs Boston Healthcare System, Boston, MA, USA, [email protected]
Cleber A. Trujillo Departamento de Bioquímica, Instituto de Química,Universidade de São Paulo, São Paulo, Brazil, [email protected]
Henning Ulrich Departamento de Bioquímica, Instituto de Química, Universidadede São Paulo, São Paulo, Brazil, [email protected]
Dustin R. Wakeman Stem Cell and Regeneration Program, The Burnham Institute,La Jolla, CA, USA; University of California at San Diego: Graduate Program inBiomedical Sciences, La Jolla, CA 92093, USA, [email protected]
Zhigang Xue UPMC Univ Paris 6, UMR 7079, Paris, France,[email protected]
Katia K. Yuahasi Programa de Pós-graduação em Neurologia, Departamento deNeurologia e Neurocirurgia, Universidade Federal de São Paulo, São Paulo, Brazil,[email protected]
Ewa Zuba-Surma Stem Cell Institute at James Graham Brown Cancer Center,University of Louisville, Louisville, KY, USA, [email protected]