Stem cells living with a Notch

Notch signaling has been shown over the past few decades to play fundamental roles in a plethora of developmental processes in an evolutionarily conserved fashion. Notch-mediated cell-to-cell signaling is involved in many aspects of embryonic development and control of tissue homeostasis in a variety of adult tissues, and regulates stem cell maintenance, cell differentiation and cellular homeostasis. The focus of this Review is the role of Notch signaling in stem cells, comparing insights from flies, fish and mice to highlight similarities, as well as differences, between species, tissues and stem cell compartments.

[1]  H. Macdonald,et al.  Notch signaling in the immune system. , 2010, Immunity.

[2]  A. Spradling,et al.  Multipotent Drosophila Intestinal Stem Cells Specify Daughter Cell Fates by Differential Notch Signaling , 2007, Science.

[3]  L. Zon,et al.  Hematopoietic stem cell fate is established by the Notch-Runx pathway. , 2005, Genes & development.

[4]  Bruce J. Aronow,et al.  The Pan-ErbB Negative Regulator Lrig1 Is an Intestinal Stem Cell Marker that Functions as a Tumor Suppressor , 2012, Cell.

[5]  A. Brand,et al.  Transcriptional control of stem cell maintenance in the Drosophila intestine , 2010, Development.

[6]  U. Lendahl,et al.  Hypoxia requires notch signaling to maintain the undifferentiated cell state. , 2005, Developmental cell.

[7]  B. Barres,et al.  Notch Receptor Activation Inhibits Oligodendrocyte Differentiation , 1998, Neuron.

[8]  N. Galjart,et al.  In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium , 2010, Nature.

[9]  M. Rudnicki,et al.  Pax7 Is Required for the Specification of Myogenic Satellite Cells , 2000, Cell.

[10]  G. Lyons,et al.  Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. , 1994, Development.

[11]  M. Götz,et al.  Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. , 2010, Cell stem cell.

[12]  Raphael Kopan,et al.  The Canonical Notch Signaling Pathway: Unfolding the Activation Mechanism , 2009, Cell.

[13]  Jeanne Shen,et al.  A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. , 2008, Cell stem cell.

[14]  Y. Barrandon,et al.  Generation and characterization of a Notch1 signaling‐specific reporter mouse line , 2012, Genesis.

[15]  David Ish-Horowicz,et al.  Expression of a Delta homologue in prospective neurons in the chick , 1995, Nature.

[16]  Ana Cumano,et al.  Ontogeny of the hematopoietic system. , 2007, Annual review of immunology.

[17]  H. Macdonald,et al.  Hes1 is a critical but context-dependent mediator of canonical Notch signaling in lymphocyte development and transformation. , 2010, Immunity.

[18]  L. Samuelson,et al.  Mouse atonal homolog 1 directs intestinal progenitors to secretory cell rather than absorptive cell fate. , 2010, Developmental biology.

[19]  U. Suter,et al.  Notch1 is required for neuronal and glial differentiation in the cerebellum. , 2002, Development.

[20]  R. Klein,et al.  Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. , 2004, Developmental biology.

[21]  Heinrich Jasper,et al.  JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. , 2008, Cell stem cell.

[22]  D. Poulson Chromosomal Deficiencies and the Embryonic Development of Drosophila Melanogaster. , 1937, Proceedings of the National Academy of Sciences of the United States of America.

[23]  T. Enver,et al.  Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1 , 2008, The EMBO journal.

[24]  F. Schweisguth,et al.  Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine , 2011 .

[25]  T. Kadesch,et al.  The Notch Effector Hey1 Associates with Myogenic Target Genes to Repress Myogenesis* , 2009, The Journal of Biological Chemistry.

[26]  S. Ogawa,et al.  Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. , 2003, Immunity.

[27]  Francois Pognan,et al.  Modulation of notch processing by gamma-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation. , 2004, Toxicological sciences : an official journal of the Society of Toxicology.

[28]  J. Posakony,et al.  Suppressor of Hairless, the Drosophila homolog of the mouse recombination signal-binding protein gene, controls sensory organ cell fates , 1992, Cell.

[29]  E. Kremmer,et al.  RBPJκ-Dependent Signaling Is Essential for Long-Term Maintenance of Neural Stem Cells in the Adult Hippocampus , 2010, The Journal of Neuroscience.

[30]  Hans Clevers,et al.  Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4 , 1998, Nature Genetics.

[31]  P. Dempsey,et al.  Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells , 2012, Development.

[32]  D. Scadden,et al.  Osteoblastic cells regulate the haematopoietic stem cell niche , 2003, Nature.

[33]  V. Hartenstein,et al.  Development of the Drosophila entero-endocrine lineage and its specification by the Notch signaling pathway. , 2011, Developmental biology.

[34]  L. Zon,et al.  Use of the zebrafish system to study primitive and definitive hematopoiesis. , 2005, Annual review of genetics.

[35]  Kathryn E. Crosier,et al.  Live imaging of Runx1 expression in the dorsal aorta tracks the emergence of blood progenitors from endothelial cells. , 2010, Blood.

[36]  S. Artavanis-Tsakonas,et al.  The Notch locus and the cell biology of neuroblast segregation. , 1991, Annual review of cell biology.

[37]  S. Artavanis-Tsakonas,et al.  Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine , 2009, Proceedings of the National Academy of Sciences.

[38]  T. Rando,et al.  Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. , 2012, Cell stem cell.

[39]  B. Black,et al.  Activated Notch Inhibits Myogenic Activity of the MADS-Box Transcription Factor Myocyte Enhancer Factor 2C , 1999, Molecular and Cellular Biology.

[40]  L. Espinosa,et al.  Hematopoietic stem cells: to be or Notch to be. , 2012, Blood.

[41]  G. Fishell,et al.  Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. , 2001, Development.

[42]  W. Harris,et al.  Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos , 1993, Cell.

[43]  A. Wagers,et al.  Notch signaling in the regulation of stem cell self-renewal and differentiation. , 2010, Current topics in developmental biology.

[44]  K. Moriyoshi,et al.  Persistent expression of helix‐loop‐helix factor HES‐1 prevents mammalian neural differentiation in the central nervous system. , 1994, The EMBO journal.

[45]  C. Keller,et al.  Constitutive Notch Activation Upregulates Pax7 and Promotes the Self-Renewal of Skeletal Muscle Satellite Cells , 2012, Molecular and Cellular Biology.

[46]  Robert D. Kirch,et al.  Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self‐renewal , 2005, The EMBO journal.

[47]  Elaine Dzierzak,et al.  Runx1 is required for the endothelial to hematopoietic cell transition but not thereafter , 2009, Nature.

[48]  Y. Kong,et al.  Mind bomb-1 Is Essential for Intraembryonic Hematopoiesis in the Aortic Endothelium and the Subaortic Patches , 2008, Molecular and Cellular Biology.

[49]  Freddy Radtke,et al.  Paradigms of Notch Signaling in Mammals , 2005 .

[50]  M. Bate,et al.  A dual requirement for neurogenic genes in Drosophila myogenesis. , 1993, Development.

[51]  T. Pierfelice,et al.  Notch in the Vertebrate Nervous System: An Old Dog with New Tricks , 2011, Neuron.

[52]  Caroline L. Speck,et al.  Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer. , 2007, Blood.

[53]  S. Bray Notch signalling: a simple pathway becomes complex , 2006, Nature Reviews Molecular Cell Biology.

[54]  S. Bray,et al.  Notch signalling in Drosophila: three ways to use a pathway. , 1998, Seminars in cell & developmental biology.

[55]  S. Ogawa,et al.  AML1/Runx1 rescues Notch1-null mutation-induced deficiency of para-aortic splanchnopleural hematopoiesis. , 2006, Blood.

[56]  I. Bernstein,et al.  Notch2 governs the rate of generation of mouse long- and short-term repopulating stem cells. , 2011, The Journal of clinical investigation.

[57]  D. Scadden,et al.  Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. , 2002, Blood.

[58]  J. Sklar,et al.  TAN-1, the human homolog of the Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms , 1991, Cell.

[59]  I. Bernstein,et al.  Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling , 2000, Nature Medicine.

[60]  M. Capecchi,et al.  Bmi 1 is expressed in vivo in intestinal stem cells , 2010 .

[61]  M. Bhatia,et al.  The Notch Ligand Jagged-1 Represents a Novel Growth Factor of Human Hematopoietic Stem Cells , 2000, The Journal of experimental medicine.

[62]  Su Guo,et al.  Intralineage Directional Notch Signaling Regulates Self-Renewal and Differentiation of Asymmetrically Dividing Radial Glia , 2012, Neuron.

[63]  Y. Kong,et al.  Mind Bomb 1-Expressing Intermediate Progenitors Generate Notch Signaling to Maintain Radial Glial Cells , 2008, Neuron.

[64]  C. Cepko,et al.  Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. , 1995, Development.

[65]  C. Cepko,et al.  The Expression and Function of Notch Pathway Genes in the Developing Rat Eye , 1997, The Journal of Neuroscience.

[66]  J. Aster,et al.  Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. , 2005, Cell stem cell.

[67]  Haiyang Huang,et al.  Identification of the haematopoietic stem cell niche and control of the niche size , 2003, Nature.

[68]  A. Brand,et al.  Regulating the balance between symmetric and asymmetric stem cell division in the developing brain , 2011, Fly.

[69]  H. Clevers,et al.  Identification of stem cells in small intestine and colon by marker gene Lgr5 , 2007, Nature.

[70]  M. Capecchi,et al.  The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations , 2011, Proceedings of the National Academy of Sciences.

[71]  F. Schweisguth,et al.  Asymmetric localization and function of cell-fate determinants: a fly’s view , 2004, Current Opinion in Neurobiology.

[72]  Gayle M. Smythe,et al.  Notch-Mediated Restoration of Regenerative Potential to Aged Muscle , 2003, Science.

[73]  Tom H. Cheung,et al.  Notch Signaling Is Necessary to Maintain Quiescence in Adult Muscle Stem Cells , 2012, Stem cells.

[74]  M. Rudnicki,et al.  MyoD or Myf-5 is required for the formation of skeletal muscle , 1993, Cell.

[75]  Hans Clevers,et al.  Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts , 2011, Nature.

[76]  Heinrich Jasper,et al.  EGF signaling regulates the proliferation of intestinal stem cells in Drosophila , 2011, Development.

[77]  H. Clevers,et al.  Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche , 2009, Nature.

[78]  S. Artavanis-Tsakonas,et al.  Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process , 2003, Development.

[79]  Y. Jan,et al.  Genetic control of cell fate specification in Drosophila peripheral nervous system. , 1994, Annual review of genetics.

[80]  Daniel J. Hoeppner,et al.  Notch signalling regulates stem cell numbers in vitro and in vivo , 2006, Nature.

[81]  Olivier Pourquié,et al.  Maintenance of neuroepithelial progenitor cells by Delta–Notch signalling in the embryonic chick retina , 1997, Current Biology.

[82]  Hans Clevers,et al.  Lrig1 controls intestinal stem cell homeostasis by negative regulation of ErbB signalling , 2012, Nature Cell Biology.

[83]  K. Kaestner,et al.  Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. , 2011, Gastroenterology.

[84]  C. Tabin,et al.  Somitic origin of limb muscle satellite and side population cells. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[85]  S. Artavanis-Tsakonas,et al.  Notch signals control the fate of immature progenitor cells in the intestine , 2005, Nature.

[86]  E. Kremmer,et al.  Notch Activity Levels Control the Balance between Quiescence and Recruitment of Adult Neural Stem Cells , 2010, The Journal of Neuroscience.

[87]  S. Artavanis-Tsakonas,et al.  Notch Lineages and Activity in Intestinal Stem Cells Determined by a New Set of Knock-In Mice , 2011, PloS one.

[88]  David Ish-Horowicz,et al.  Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta , 1995, Nature.

[89]  Pasko Rakic,et al.  Not(ch) just development: Notch signalling in the adult brain , 2011, Nature Reviews Neuroscience.

[90]  M. Gering,et al.  Hey2 acts upstream of Notch in hematopoietic stem cell specification in zebrafish embryos. , 2010, Blood.

[91]  J. Campos-Ortega,et al.  The molecular genetics of early neurogenesis in Drosophila melanogaster , 1989, BioEssays : news and reviews in molecular, cellular and developmental biology.

[92]  D. Castel,et al.  A Critical Requirement for Notch Signaling in Maintenance of the Quiescent Skeletal Muscle Stem Cell State , 2012, Stem cells.

[93]  K. Kissa,et al.  Blood stem cells emerge from aortic endothelium by a novel type of cell transition , 2010, Nature.

[94]  Ryoichiro Kageyama,et al.  The role of Hes genes in intestinal development, homeostasis and tumor formation , 2012, Development.

[95]  J. L. de la Pompa,et al.  RBPjκ-dependent Notch function regulates Gata2 and is essential for the formation of intra-embryonic hematopoietic cells , 2005 .

[96]  Tasuku Honjo,et al.  Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. , 2004, Genes & development.

[97]  Janet Rossant,et al.  Dosage-sensitive requirement for mouse Dll4 in artery development. , 2004, Genes & development.

[98]  J. Sundberg,et al.  Notch signaling is essential for vascular morphogenesis in mice. , 2000, Genes & development.

[99]  H. Zoghbi,et al.  Requirement of Math1 for Secretory Cell Lineage Commitment in the Mouse Intestine , 2001, Science.

[100]  R. Shivdasani,et al.  Genetic Evidence That Intestinal Notch Functions Vary Regionally and Operate through a Common Mechanism of Math1 Repression* , 2011, The Journal of Biological Chemistry.

[101]  Hans Clevers,et al.  Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2 , 2008, EMBO reports.

[102]  Hans Clevers,et al.  Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. , 2003, Genes & development.

[103]  Shahragim Tajbakhsh,et al.  Pax3/Pax7 mark a novel population of primitive myogenic cells during development. , 2005, Genes & development.

[104]  A. Mansouri,et al.  A Pax3/Pax7-dependent population of skeletal muscle progenitor cells , 2005, Nature.

[105]  A. Martinez-Arias,et al.  Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells , 2012, The EMBO journal.

[106]  A. Spradling,et al.  The adult Drosophila posterior midgut is maintained by pluripotent stem cells , 2006, Nature.

[107]  Barbara Gayraud-Morel,et al.  Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice , 2004, Nature.

[108]  A. Parfitt,et al.  Bone remodeling. , 1988, Henry Ford Hospital medical journal.

[109]  H. Okamoto,et al.  Dual Roles of Notch in Regulation of Apically Restricted Mitosis and Apicobasal Polarity of Neuroepithelial Cells , 2011, Neuron.

[110]  U. Lendahl,et al.  Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation , 2003, Development.

[111]  J. Knoblich,et al.  Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. , 2009, Genes & development.

[112]  Colleen Delaney,et al.  Notch-mediated expansion of human cord blood progenitor cells capable of rapid myeloid reconstitution , 2010, Nature Medicine.

[113]  T. Ohtsuka,et al.  Roles of the Basic Helix-Loop-Helix Genes Hes1 and Hes5 in Expansion of Neural Stem Cells of the Developing Brain* , 2001, The Journal of Biological Chemistry.

[114]  R. Sambasivan,et al.  Skeletal muscle stem cell birth and properties. , 2007, Seminars in cell & developmental biology.

[115]  G. Lyons,et al.  Mef 2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis , 1994 .

[116]  D. Stainier,et al.  Hematopoietic stem cells derive directly from aortic endothelium during development , 2009, Nature.

[117]  O. Klein,et al.  A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable , 2011, Nature.

[118]  I. Nakano,et al.  Patterns of Jagged1, Jagged2, Delta‐like 1 and Delta‐like 3 expression during late embryonic and postnatal brain development suggest multiple functional roles in progenitors and differentiated cells , 2004, Journal of neuroscience research.

[119]  Cheol‐Hee Kim,et al.  Mind bomb 1 is essential for generating functional Notch ligands to activate Notch , 2005, Development.

[120]  P. Heitzler Biodiversity and noncanonical Notch signaling. , 2010, Current topics in developmental biology.

[121]  U. Suter,et al.  Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. , 2005, Blood.

[122]  J. Boulter,et al.  Jagged: A mammalian ligand that activates notch1 , 1995, Cell.

[123]  R. Bronson,et al.  Essential Role of Endothelial Notch1 in Angiogenesis , 2005, Circulation.

[124]  A. Gossler,et al.  Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants , 2007, Proceedings of the National Academy of Sciences.

[125]  J. Morgan,et al.  BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells , 2011, Cell Death and Differentiation.

[126]  Gord Fishell,et al.  Radial Glial Identity Is Promoted by Notch1 Signaling in the Murine Forebrain , 2000, Neuron.

[127]  N. Xu,et al.  EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. , 2011, Developmental biology.

[128]  Hans Clevers,et al.  Notch/γ-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells , 2005, Nature.

[129]  V. Gallo,et al.  Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal , 2010, Nature.

[130]  B. Hadland,et al.  A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. , 2004, Blood.

[131]  Manfred Gessler,et al.  The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. , 2004, Genes & development.

[132]  D. Stainier,et al.  Notch Signaling Functions as a Cell-Fate Switch between the Endothelial and Hematopoietic Lineages , 2009, Current Biology.

[133]  J. Epstein,et al.  RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells , 2007, Proceedings of the National Academy of Sciences.

[134]  K. Mori,et al.  Essential Roles of Notch Signaling in Maintenance of Neural Stem Cells in Developing and Adult Brains , 2010, The Journal of Neuroscience.

[135]  D. Traver,et al.  An environmental Wnt16/Notch pathway specifies haematopoietic stem cells , 2011, Nature.

[136]  Ian A. White,et al.  Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. , 2010, Cell stem cell.

[137]  N. Perrimon,et al.  Evidence that stem cells reside in the adult Drosophila midgut epithelium , 2006, Nature.

[138]  M. Buckingham,et al.  Distinct and dynamic myogenic populations in the vertebrate embryo. , 2009, Current opinion in genetics & development.

[139]  I. Bernstein,et al.  A human homologue of the Drosophila developmental gene, Notch, is expressed in CD34+ hematopoietic precursors. , 1994, Blood.

[140]  S. Morrison,et al.  Physiological Notch signaling promotes gliogenesis in the developing peripheral and central nervous systems , 2007, Development.

[141]  E. Bongarzone,et al.  Notch Signaling in Astrocytes and Neuroblasts of the Adult Subventricular Zone in Health and after Cortical Injury , 2006, Developmental Neuroscience.

[142]  Larry Kedes,et al.  HES and HERP families: Multiple effectors of the notch signaling pathway , 2003, Journal of cellular physiology.

[143]  H. Hirata,et al.  The Basic Helix-Loop-Helix Genes Hesr1/Hey1 and Hesr2/Hey2 Regulate Maintenance of Neural Precursor Cells in the Brain* , 2003, Journal of Biological Chemistry.

[144]  T. Honjo,et al.  The Drosophila homolog of the immunoglobulin recombination signal-binding protein regulates peripheral nervous system development , 1992, Cell.

[145]  B. Malissen,et al.  Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration , 2011, Development.

[146]  H. Macdonald,et al.  Deficient T cell fate specification in mice with an induced inactivation of Notch1. , 1999, Immunity.

[147]  Hae-Chul Park,et al.  Delta-Notch signaling regulates oligodendrocyte specification , 2003, Development.

[148]  H. Weintraub,et al.  The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. , 1994, Development.

[149]  S. Hou,et al.  JAK–STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells , 2010, Journal of cellular biochemistry.

[150]  H. Baier,et al.  Regulation of Neurogenesis by Interkinetic Nuclear Migration through an Apical-Basal Notch Gradient , 2008, Cell.

[151]  H. Rahn,et al.  Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals. , 2012, Developmental cell.

[152]  M. Fortini Introduction--Notch in development and disease. , 2012, Seminars in cell & developmental biology.

[153]  I. Bernstein,et al.  Combined effects of Notch signaling and cytokines induce a multiple log increase in precursors with lymphoid and myeloid reconstituting ability. , 2003, Blood.

[154]  Cheol‐Hee Kim,et al.  Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. , 2003, Developmental cell.