Skip to main content
SpringerLink
Log in

Insulin-dependent Non-canonical Activation of Notch in Drosophila: A Story of Notch-Induced Muscle Stem Cell Proliferation

  • Chapter
  • First Online:
Notch Signaling in Embryology and Cancer

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1227))

Abstract

Notch plays multiple roles both in development and in adult tissue homeostasis. Notch was first identified in Drosophila in which it has then been extensively studied. Among the flag-ship Notch functions we could mention its capacity to keep precursor and stem cells in a nondifferentiated state but also its ability to activate cell proliferation that in some contexts could led to cancer. In general, both these functions involve, canonical, ligand-dependent Notch activation. However, a ligand-independent Notch activation has also been described in a few cellular contexts. Here, we focus on one of such contexts, Drosophila muscle stem cells, called AMPs, and discuss how insulin-dependent noncanonical activation of Notch pushes quiescent AMPs to proliferation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138:3593–3612

    Article  CAS  PubMed  Google Scholar 

  • Aradhya R, Zmojdzian M, Da Ponte JP, Jagla K (2015) Muscle niche-driven insulin-Notch-Myc cascade reactivates dormant adult muscle precursors in Drosophila. elife 4:e08497

    Article  PubMed  PubMed Central  Google Scholar 

  • Artavanis-Tsakonas S, Matsuno K, Fortini ME (1995) Notch signaling. Science 268(5208):225–232

    Article  CAS  PubMed  Google Scholar 

  • Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284(5415):770–776

    Article  CAS  PubMed  Google Scholar 

  • Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA (2002) Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159(1):123–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Austin J, Kimble J (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51(4):589–599

    Article  CAS  PubMed  Google Scholar 

  • Baker M (2009) Diet and insulin in a stem cell niche. Nat Rep Stem Cells. https://www.nature.com/articles/stemcells.2009.19#citeas

  • Bate M, Rushton E, Currie DA (1991) Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113(1):79–89

    CAS  PubMed  Google Scholar 

  • Bate M, Rushton E, Frasch M (1993) A dual requirement for neurogenic genes in Drosophila myogenesis. Development:149–161

    Google Scholar 

  • Bergmans BA, De Strooper B (2010) gamma-secretases: from cell biology to therapeutic strategies. Lancet Neurol 9(2):215–226

    Article  CAS  PubMed  Google Scholar 

  • Bernard S, Eilers M (2006) Control of cell proliferation and growth by Myc proteins. Results Probl Cell Differ 42:329–342

    Article  CAS  PubMed  Google Scholar 

  • Bernard F, Krejci A, Housden B, Adryan B, Bray SJ (2010) Specificity of Notch pathway activation: twist controls the transcriptional output in adult muscle progenitors. Development 137:2633–2642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bevan P (2001) Cell science at a glance, insulin signaling. J Cell Sci 114:1429–1430

    CAS  PubMed  Google Scholar 

  • Bigas A, Espinosa L (2018) The multiple usages of Notch signaling in development, cell differentiation and cancer. Curr Opin Cell Biol 55:1–7

    Article  CAS  PubMed  Google Scholar 

  • Billiard F et al (2018) Delta-like ligand-4-notch signaling inhibition regulates pancreatic islet function and insulin secretion. Cell Rep 22(4):895–904

    Article  CAS  PubMed  Google Scholar 

  • Blochlinger K, Bodmer R, Jan LY, Jan YN (1990) Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev 4:1322–1331

    Article  CAS  PubMed  Google Scholar 

  • Blochlinger K, Jan LY, Jan YN (1993) Post-embryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117:441–450

    CAS  PubMed  Google Scholar 

  • Bolós V, Grego-Bessa J, de la Pompa JL (2007) Notch signaling in development and cancer. Endocr Rev 28(3):339–363

    Article  PubMed  CAS  Google Scholar 

  • Boppart MD, De Lisio M, Zou K, Huntsman HD (2013) Defining a role for non-satellite stem cells in the regulation of muscle repair following exercise. Front Physiol 4:310

    Article  PubMed  PubMed Central  Google Scholar 

  • Borggrefe T, Oswald F (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 66(10):1631–1646

    Article  CAS  PubMed  Google Scholar 

  • Boucher J, Kleinridders A, Kahn CR (2014) Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harb Perspect Biol 6(1)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boukhatmi H, Bray S (2018) A population of adult satellite-like cells in Drosophila is maintained through a switch in RNA-isoforms. elife 7:e35954

    Article  PubMed  PubMed Central  Google Scholar 

  • Boyette LB, Tuan RS (2014) Adult stem cells and diseases of aging. J Clin Med 3(1):88–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozkulak EC, Weinmaster G (2009) Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling. Mol Cell Biol 29(21):5679–5695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118(2):401–415

    CAS  PubMed  Google Scholar 

  • Bray SJ (2006) Notch signaling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7(9):678–689

    Article  CAS  PubMed  Google Scholar 

  • Bretones G, Delgado MD, León J (2015) Myc and cell cycle control. Biochim Biophys Acta 1849(5):506–516

    Article  CAS  PubMed  Google Scholar 

  • Broadie KS, Bate M (1991) The development of adult muscles in Drosophila: ablation of identified muscle precursor cells. Development 113(1):103–118

    CAS  PubMed  Google Scholar 

  • Carmena A, Bate M, Jimenez F (1995) Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev 9(19):2373–2383

    Article  CAS  PubMed  Google Scholar 

  • Cavaliere V, Donati A, Hsouna A, Hsu T, Gargiulo G (2005) dAkt kinase controls follicle cell size during Drosophila oogenesis. Dev Dyn 232(3):845–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaturvedi D, Reichert H, Gunage RD, VijayRaghavan K (2017) Identification and functional characterization of muscle satellite cells in Drosophila. elife 6:e30107

    Article  PubMed  PubMed Central  Google Scholar 

  • Chell JM, Brand AH (2010) Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143(7):1161–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chou HL, Hsu HJ (2017) Age regulates Drosophila ovarian germline stem cells via insulin-dependent and independent mechanisms. J Cell Signal 2:174

    Google Scholar 

  • Conboy IM, Rando TA (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3(3):397–409

    Article  CAS  PubMed  Google Scholar 

  • Conrad C, Huss R (2005) Adult stem cell lines in regenerative medicine and reconstructive surgery. J Surg Res 124(2):201–208

    Article  PubMed  Google Scholar 

  • Crisan M et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3(3):301–313

    Article  CAS  PubMed  Google Scholar 

  • D’Souza B, Miyamoto A, Weinmaster G (2008) The many facets of Notch ligands. Oncogene 27(38):5148–5167

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • D’Souza B, Meloty-Kapella L, Weinmaster G (2010) Canonical and non-canonical Notch ligands. Curr Top Dev Biol 92:73–129

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Meyts P (2016) The insulin receptor and its signal transduction network. Endotext. MDText.com, Inc, South Dartmouth, MA

    Google Scholar 

  • Dexter JS (1914) The analysis of a case of continuous variation in Drosophila by a study of its linkage relations. Am Nat 48:712–758

    Article  Google Scholar 

  • Eliazer S, Buszczak M (2011) Finding a niche: studies from the Drosophila ovary. Stem Cell Res Ther 2(6):45

    Article  PubMed  PubMed Central  Google Scholar 

  • Farber E (1995) Cell proliferation as a major risk factor for cancer: a concept of doubtful validity. Cancer Res 55:3759–3762

    CAS  PubMed  Google Scholar 

  • Feitelson MA, Arzumanyan A, Kulathinal RJ, et al (2015) Sustained proliferation in cancer: mechanisms and novel therapeutic targets. Semin Cancer Biol 35 Suppl(Suppl):S25–S54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Figeac N, Jagla T, Aradhya R, Da Ponte JP, Jagla K (2010) Drosophila adult muscle precursors form a network of interconnected cells and are specified by the rhomboid-triggered EGF pathway. Development 137(12):1965–1973

    Article  CAS  PubMed  Google Scholar 

  • Foronda D, Weng R, Verma P, Chen YW, Cohen SM (2014) Coordination of insulin and Notch pathway activities by microRNA miR-305 mediates adaptive homeostasis in the intestinal stem cells of the Drosophila gut. Genes Dev 28(21):2421–2431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fortini ME (2009) Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 16(5):633–647

    Article  CAS  PubMed  Google Scholar 

  • Furman DP, Bukharina TA (2008) How Drosophila melanogaster forms its mechanoreceptors. Curr Genomics 9(5):312–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallant P (2013) Myc function in Drosophila. Cold Spring Harb Perspect Med 3(10):a014324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gancz D, Gilboa L (2013) Insulin and target of rapamycin signaling orchestrate the development of ovarian niche-stem cell units in Drosophila. Development 140:4145–4154

    Article  CAS  PubMed  Google Scholar 

  • Go MJ, Artavanis-Tsakonas S (1998) A genetic screen for novel components of the notch signaling pathway during Drosophila bristle development. Genetics 150(1):211–220

    CAS  PubMed  PubMed Central  Google Scholar 

  • Go MJ, Eastman DS, Artavanis-Tsakonas S (1998) Cell proliferation control by Notch signaling in Drosophila development. Development 125:2031–2040

    CAS  PubMed  Google Scholar 

  • Gordon WR, Arnett KL, Blacklow SC (2008) The molecular logic of Notch signaling—a structural and biochemical perspective. J Cell Sci 121(Pt 19):3109–3119

    Article  CAS  PubMed  Google Scholar 

  • Gordon WR, Roy M, Vardar-Ulu D, Garfinkel M, Mansour MR, Aster JC, Blacklow SC (2009) Structure of the Notch1-negative regulatory region: implications for normal activation and pathogenic signaling in T-ALL. Blood 113(18):4381–4390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenwald I (1998) LIN-12/Notch signaling: lessons from worms and flies. Genes Dev 12(12):1751–1762

    Article  CAS  PubMed  Google Scholar 

  • Greenwald IS, Sternberg PW, Horvitz HR (1983) The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34(2):435–444

    Article  CAS  PubMed  Google Scholar 

  • Grewal SS (2009) Insulin/TOR signaling in growth and homeostasis: a view from the fly world. Int J Biochem Cell Biol 41(5):1006–1010

    Article  CAS  PubMed  Google Scholar 

  • Grotek B, Wehner D, Weidinger G (2013) Notch signaling coordinates cellular proliferation with differentiation during zebrafish fin regeneration. Development 140:1412–1423

    Article  CAS  PubMed  Google Scholar 

  • Gunage RD, Dhanyasi N, Reichert H, Raghavan KV (2017) Drosophila adult muscle development and regeneration. Semin Cell Dev Biol 72:56–66

    Article  CAS  PubMed  Google Scholar 

  • Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, Flint AF, Kunkel LM, Mulligan RC (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401(6751):390–394

    CAS  PubMed  Google Scholar 

  • Ho DM, Artavanis-Tsakonas S (2016) The Notch-mediated proliferation circuitry. Curr Top Dev Biol 116:17–33

    Article  CAS  PubMed  Google Scholar 

  • Homem CCF, Knoblich JA (2012) Drosophila neuroblasts: a model for stem cell biology. Development 139:4297–4310

    Article  CAS  PubMed  Google Scholar 

  • Hori K, Sen A, Kirchhausen T, Artavanis-Tsakonas S (2012) Regulation of ligand-independent Notch signal through intracellular trafficking. Commun Integr Biol 5(4):374–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hori K, Sen A, Artavanis-Tsakonas S (2013) Notch signaling at a glance. J Cell Sci 126:2135–2140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu H-J, Drummond-Barbosa D (2009) Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proc Nat Acad Sci 106(4):1117–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang F, Dambly-Chaudiere C, Ghysen A (1991) The emergence of sense organs in the wing disc of Drosophila. Development 111:1087–1095

    CAS  PubMed  Google Scholar 

  • Kannan K, Fridell YW (2013) Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction. Front Physiol 4:288

    Article  PubMed  PubMed Central  Google Scholar 

  • Katz B (1961) The terminations of the afferent nerve fibre in the muscle spindle of the frog. Philos Trans R Soc Lond Ser B Biol Sci 243:221–240

    Google Scholar 

  • Kidd S, Kelley MR, Young MW (1986) Sequence of the notch locus of Drosophila melanogaster: relationship of the encoded protein to mammalian clotting and growth factors. Mol Cell Biol 6(9):3094–3108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch U, Lehal R, Radtke F (2013) Stem cells living with a Notch. Development 140:689–704

    Article  CAS  PubMed  Google Scholar 

  • Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137(2):216–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Körbling M, Estrov Z, Champlin R (2003) Adult stem cells and tissue repair. Bone Marrow Transplant 32:S23–S24

    Article  PubMed  CAS  Google Scholar 

  • Krafts KP (2010) Tissue repair: the hidden drama. Organogenesis 6(4):225–233

    Article  PubMed  PubMed Central  Google Scholar 

  • LaFever L, Feoktistov A, Hsu H-J, Drummond-Barbosa D (2010) Specific roles of target of rapamycin in the control of stem cells and their progeny in the Drosophila ovary. Development 137:2117–2126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HK, Lundell MJ (2007) Differentiation of the Drosophila serotonergic lineage depends on the regulation of Zfh-1 by Notch and Eagle. Mol Cell Neurosci 36(1):47–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138:3639–3646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Wolfe MS, Selkoe DJ (2009) Toward structural elucidation of the gamma-secretase complex. Structure 17(3):326–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieber T, Kidd S, Alcamo E, Corbin V, Young MW (1993) Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev 7(10):1949–1965

    Article  CAS  PubMed  Google Scholar 

  • Liotta D, Han J, Elgar S, Garvey C, Han Z, Taylor MV (2007) The Him gene reveals a balance of inputs controlling muscle differentiation in Drosophila. Curr Biol 17(16):1409–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Sato C, Cerletti M, Wagers A (2010) Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 92:367–409

    Article  CAS  PubMed  Google Scholar 

  • Lu B, Rothenberg M, Jan LY, Jan YN (1998) Partner of Numb colocalizes with Numb during mitosis and directs Numb asymmetric localization in Drosophila neural and muscle progenitors. Cell 95(2):225–235

    Article  CAS  PubMed  Google Scholar 

  • Majka SM, Jackson KA, Kienstra KA, Majesky MW, Goodell MA, Hirschi KK (2003) Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest 111(1):71–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCarthy JJ et al (2011) Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138:3657–3666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes CC, Mirth CK (2016) Stage-specific plasticity in ovary size is regulated by insulin/insulin-like growth factor and ecdysone signaling in Drosophila. Genetics 202(2):703–719

    Article  CAS  PubMed  Google Scholar 

  • Montagnani S, Rueger MA, Hosoda T, Nurzynska D (2016) Adult stem cells in tissue maintenance and regeneration. Stem Cells Int 2016:7362879

    Article  PubMed  PubMed Central  Google Scholar 

  • Morgan TH (1917) The theory of the gene. Am Nat 51(609):513–544

    Article  Google Scholar 

  • Morgan T (1928) The theory of the gene (revised ed.). Yale University Press, New Haven, pp 77–81

    Google Scholar 

  • Mumm JS, Schroeter EH, Saxena MT, Griesemer A, Tian X, Pan DJ et al (2000) A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol Cell 5(2):197–206

    Article  CAS  PubMed  Google Scholar 

  • Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G (2011) Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138:3625–3637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nässel DR, Liu Y, Luo J (2015) Insulin/IGF signaling and its regulation in Drosophila. Gen Comp Endocrinol 15(221):255–266

    Article  CAS  Google Scholar 

  • Ninov N, Borius M, Stainier DYR (2012) Different levels of Notch signaling regulate quiescence, renewal and differentiation in pancreatic endocrine progenitors. Development 139:1557–1567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okochi M, Steiner H, Fukumori A, Tanii H, Tomita T, Tanaka T et al (2002) Presenilins mediate a dual intramembranous gamma-secretase cleavage of Notch-1. EMBO J 21(20):5408–5416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer WH, Deng WM (2015) Ligand-independent mechanisms of notch activity. Trends Cell Biol 25(11):697–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penton AL, Leonard LD, Spinner NB (2012) Notch signaling in human development and disease. Semin Cell Dev Biol 23(4):450–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perdigoto CN, Schweisguth F, Bardin AJ (2011) Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine. Development 138:4585–4595

    Article  CAS  PubMed  Google Scholar 

  • Prentice DA (2019) Adult stem cells; successful standard for regenerative medicine. Cir Res 124:837–839

    Article  CAS  Google Scholar 

  • Priess JR, Schnabel H, Schnabel R (1987) The glp-1 locus and cellular interactions in early C. elegans embryos. Cell 51(4):601–611

    Article  CAS  PubMed  Google Scholar 

  • Puretskaia OA, Albert EA, Terekhanova N, Bökel C (2017) Micromanagment of stem cell proliferation by the Drosophila testis stem cell niche. BioRxiv

    Google Scholar 

  • Rebay I, Fehon RG, Artavanis-Tsakonas S (1993) Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74(2):319–329

    Article  CAS  PubMed  Google Scholar 

  • Rebeiz M, Reeves NL, Posakony JW (2002) SCORE: a computational approach to the identification of cis-regulatory modules and target genes in whole-genome sequence data. Proc Natl Acad Sci 99(15):9888–9893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139:2845–2856

    Article  CAS  PubMed  Google Scholar 

  • Roegiers F, Jan YN (2004) Asymmetric cell division. Curr Opin Cell Biol 16(2):195–205

    Article  CAS  PubMed  Google Scholar 

  • Roy S, VijayRaghavan K (1999) Muscle pattern diversification in Drosophila: the story of imaginal myogenesis. BioEssays 21(6):486–498

    Article  CAS  PubMed  Google Scholar 

  • Rumman M, Dhawan J, Kassem M (2015) Concise review: quiescence in adult stem cells: biological significance and relevance to tissue regeneration. Stem Cells 33(10):2903–2912

    Article  PubMed  Google Scholar 

  • Rushton E, Drysdale RA, Abmayr SM, Michelson AM, Bate M (1995) Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121(7):1979–1988

    CAS  PubMed  Google Scholar 

  • Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, Gayraud-Morel B, Guenou H, Malissen B, Tajbakhsh S, Galy A (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138:3647–3656

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Irizarry C, Carpenter AC, Weng AP, Pear WS, Aster JC, Blacklow SC (2004) Notch subunit heterodimerization and prevention of ligand-independent proteolytic activation depend, respectively, on a novel domain and the LNR repeats. Mol Cell Biol 24(21):9265–9273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato C, Zhao G, Ilagan MX (2012) An overview of notch signaling in adult tissue renewal and maintenance. Curr Alzheimer Res 9(2):227–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786

    Article  CAS  PubMed  Google Scholar 

  • Sharma M, Garber A, Farmer J (2008) Role of insulin signaling in maintaining energy homeostasis. Endocr Pract 14(3):373–380

    Article  PubMed  Google Scholar 

  • Sousa-Nunes R, Yee LL, Gould AP (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471(7339):508–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinbuck MP, Susan W (2018) A review of notch processing with new insights into ligand-independent notch signaling in T-cells. Front Immunol 9:1230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sudarsan V, Anant S, Guptan P, VijayRaghavan K, Skaer H (2001) Myoblast diversification and ectodermal signaling in Drosophila. Dev Cell 1(6):829–839

    Article  CAS  PubMed  Google Scholar 

  • Thomas BJ (2005) Cell-cycle control during development, taking it up a Notch. Dev Cell 8:451–459

    Article  CAS  PubMed  Google Scholar 

  • Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12(2):143–152

    Article  CAS  PubMed  Google Scholar 

  • Valenti L, Mendoza RM, Rametta R, Maggioni M, Kitajewski C, Shawber CJ, Pajvani UC (2013) Hepatic Notch signaling correlates with insulin resistance and nonalcoholic fatty liver disease. Diabetes 62(12):4052–4062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Tetering G, van Diest P, Verlaan I, van der Wall E, Kopan R, Vooijs M (2009) Metalloprotease ADAM10 is required for Notch1 site 2 cleavage. J Biol Chem 284(45):31018–31027

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang YX, Rudnicki MA (2012) Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 13:127–133

    Article  CAS  Google Scholar 

  • Wharton KA, Johansen KM, Xu T, Artavanis-Tsakonas S (1985) Nucleotide sequence from the neurogenic locus notch implies a gene product that shares homology with proteins containing EGF-like repeats. Cell 43(3 Pt 2):567–581

    Article  CAS  PubMed  Google Scholar 

  • Wirtz-Peitz F, Nishimura T, Knoblich JA (2008) Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 135(1):161–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong W, Jiang MM, Weinmaster G, Jan LY, Jan YN (1997) Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 124(10):1887–1897

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biotechnology, Amrita Vishwa Vidya Peetham, Amritapuri, Vallikavu, Kollam, Kerala, India

    Rajaguru Aradhya

  2. Genetics Reproduction and Development (GReD) Institute, UMR INSERM 1103, CNRS 6293, University of Clermont Auvergne, Clermont-Ferrand, France

    Krzysztof Jagla

Authors
  1. Rajaguru Aradhya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Krzysztof Jagla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Krzysztof Jagla .

Editor information

Editors and Affiliations

  1. Department of Dermatology, The Saarland University Hospital, Homburg, Saarland, Germany

    Jörg Reichrath

  2. Department of Dermatology, The Saarland University Hospital, Homburg, Saarland, Germany

    Sandra Reichrath

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Aradhya, R., Jagla, K. (2020). Insulin-dependent Non-canonical Activation of Notch in Drosophila: A Story of Notch-Induced Muscle Stem Cell Proliferation. In: Reichrath, J., Reichrath, S. (eds) Notch Signaling in Embryology and Cancer. Advances in Experimental Medicine and Biology, vol 1227. Springer, Cham. https://doi.org/10.1007/978-3-030-36422-9_9

Download citation

Publish with us

Policies and ethics

Search

Navigation