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Distant activation of Notch signaling induces stem cell niche assembly


Autoři: Andriy S. Yatsenko aff001;  Halyna R. Shcherbata aff001
Působiště autorů: Institute of Cell Biochemistry, Hannover Medical School, Hannover, Germany aff001
Vyšlo v časopise: Distant activation of Notch signaling induces stem cell niche assembly. PLoS Genet 17(3): e1009489. doi:10.1371/journal.pgen.1009489
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009489

Souhrn

Here we show that multiple modes of Notch signaling activation specify the complexity of spatial cellular interactions necessary for stem cell niche assembly. In particular, we studied the formation of the germline stem cell niche in Drosophila ovaries, which is a two-step process whereby terminal filaments are formed first. Then, terminal filaments signal to the adjacent cap cell precursors, resulting in Notch signaling activation, which is necessary for the lifelong acquisition of stem cell niche cell fate. The genetic data suggest that in order to initiate the process of stem cell niche assembly, Notch signaling is activated among non-equipotent cells via distant induction, where germline Delta is delivered to somatic cells located several diameters away via cellular projections generated by primordial germ cells. At the same time, to ensure the robustness of niche formation, terminal filament cell fate can also be induced by somatic Delta via cis- or trans-inhibition. This exemplifies a double security mechanism that guarantees that the germline stem cell niche is formed, since it is indispensable for the adjacent germline precursor cells to acquire and maintain stemness necessary for successful reproduction. These findings contribute to our understanding of the formation of stem cell niches in their natural environment, which is important for stem cell biology and regenerative medicine.

Klíčová slova:

Actins – Cell differentiation – Morphogenesis – Notch signaling – Ovaries – Precursor cells – Signal inhibition – Stem cell niche


Zdroje

1. Nandagopal N, Santat LA, LeBon L, Sprinzak D, Bronner ME, Elowitz MB. Dynamic Ligand Discrimination in the Notch Signaling Pathway. Cell. 2018;172(4):869–80 e19. Epub 2018/02/06. doi: 10.1016/j.cell.2018.01.002 29398116.

2. Shaya O, Binshtok U, Hersch M, Rivkin D, Weinreb S, Amir-Zilberstein L, et al. Cell-Cell Contact Area Affects Notch Signaling and Notch-Dependent Patterning. Dev Cell. 2017;40(5):505–11 e6. Epub 2017/03/16. doi: 10.1016/j.devcel.2017.02.009 28292428; PubMed Central PMCID: PMC5435110.

3. Sprinzak D, Lakhanpal A, LeBon L, Garcia-Ojalvo J, Elowitz MB. Mutual inactivation of Notch receptors and ligands facilitates developmental patterning. PLoS Comput Biol. 2011;7(6):e1002069. Epub 2011/06/23. doi: 10.1371/journal.pcbi.1002069 21695234; PubMed Central PMCID: PMC3111533.

4. Fiuza UM, Arias AM. Cell and molecular biology of Notch. J Endocrinol. 2007;194(3):459–74. doi: 10.1677/JOE-07-0242 17761886.

5. Le Borgne R, Bardin A, Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development. 2005;132(8):1751–62. Epub 2005/03/26. 132/8/1751 [pii] doi: 10.1242/dev.01789 15790962.

6. Lai EC. Notch signaling: control of cell communication and cell fate. Development. 2004;131(5):965–73. Epub 2004/02/20. doi: 10.1242/dev.01074 14973298.

7. Petrovic J, Formosa-Jordan P, Luna-Escalante JC, Abello G, Ibanes M, Neves J, et al. Ligand-dependent Notch signaling strength orchestrates lateral induction and lateral inhibition in the developing inner ear. Development. 2014;141(11):2313–24. doi: 10.1242/dev.108100 24821984.

8. Kushwah R, Guezguez B, Lee JB, Hopkins CI, Bhatia M. Pleiotropic roles of Notch signaling in normal, malignant, and developmental hematopoiesis in the human. EMBO Rep. 2014;15(11):1128–38. doi: 10.15252/embr.201438842 25252682; PubMed Central PMCID: PMC4253487.

9. Vanorny DA, Mayo KE. The role of Notch signaling in the mammalian ovary. Reproduction. 2017;153(6):R187–R204. Epub 2017/03/12. doi: 10.1530/REP-16-0689 28283672; PubMed Central PMCID: PMC5512555.

10. Wilkinson HA, Fitzgerald K, Greenwald I. Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision. Cell. 1994;79(7):1187–98. Epub 1994/12/30. doi: 10.1016/0092-8674(94)90010-8 8001154.

11. Kovall RA, Gebelein B, Sprinzak D, Kopan R. The Canonical Notch Signaling Pathway: Structural and Biochemical Insights into Shape, Sugar, and Force. Dev Cell. 2017;41(3):228–41. Epub 2017/05/10. doi: 10.1016/j.devcel.2017.04.001 28486129; PubMed Central PMCID: PMC5492985.

12. De Joussineau C, Soule J, Martin M, Anguille C, Montcourrier P, Alexandre D. Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila. Nature. 2003;426(6966):555–9. Epub 2003/12/05. doi: 10.1038/nature02157 14654840.

13. Cohen M, Georgiou M, Stevenson NL, Miodownik M, Baum B. Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition. Dev Cell. 2010;19(1):78–89. Epub 2010/07/21. doi: 10.1016/j.devcel.2010.06.006 20643352.

14. Hunter GL, Hadjivasiliou Z, Bonin H, He L, Perrimon N, Charras G, et al. Coordinated control of Notch/Delta signalling and cell cycle progression drives lateral inhibition-mediated tissue patterning. Development. 2016;143(13):2305–10. doi: 10.1242/dev.134213 27226324; PubMed Central PMCID: PMC4958321.

15. Boukhatmi H, Martins T, Pillidge Z, Kamenova T, Bray S. Notch Mediates Inter-tissue Communication to Promote Tumorigenesis. Curr Biol. 2020. Epub 2020/04/11. doi: 10.1016/j.cub.2020.02.088 32275875.

16. Khait I, Orsher Y, Golan O, Binshtok U, Gordon-Bar N, Amir-Zilberstein L, et al. Quantitative Analysis of Delta-like 1 Membrane Dynamics Elucidates the Role of Contact Geometry on Notch Signaling. Cell Rep. 2016;14(2):225–33. Epub 2016/01/11. doi: 10.1016/j.celrep.2015.12.040 26748704.

17. del Alamo D, Rouault H, Schweisguth F. Mechanism and significance of cis-inhibition in Notch signalling. Curr Biol. 2011;21(1):R40–7. doi: 10.1016/j.cub.2010.10.034 21215938.

18. Palmer WH, Jia D, Deng WM. Cis-interactions between Notch and its ligands block ligand-independent Notch activity. Elife. 2014;3. doi: 10.7554/eLife.04415 25486593; PubMed Central PMCID: PMC4286723.

19. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, Anderson GA, et al. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature. 2010;465(7294):86–90. Epub 2010/04/27. doi: 10.1038/nature08959 20418862; PubMed Central PMCID: PMC2886601.

20. Mukherjee T, Kim WS, Mandal L, Banerjee U. Interaction between Notch and Hif-alpha in development and survival of Drosophila blood cells. Science. 2011;332(6034):1210–3. doi: 10.1126/science.1199643 21636775; PubMed Central PMCID: PMC4412745.

21. Hadjivasiliou Z, Hunter GL, Baum B. A new mechanism for spatial pattern formation via lateral and protrusion-mediated lateral signalling. J R Soc Interface. 2016;13(124). Epub 2016/11/04. doi: 10.1098/rsif.2016.0484 27807273; PubMed Central PMCID: PMC5134009.

22. Barad O, Rosin D, Hornstein E, Barkai N. Error minimization in lateral inhibition circuits. Sci Signal. 2010;3(129):ra51. doi: 10.1126/scisignal.2000857 20606215.

23. Ward EJ, Shcherbata HR, Reynolds SH, Fischer KA, Hatfield SD, Ruohola-Baker H. Stem cells signal to the niche through the Notch pathway in the Drosophila ovary. Curr Biol. 2006;16(23):2352–8. Epub 2006/10/31. doi: 10.1016/j.cub.2006.10.022 17070683.

24. Song X, Call GB, Kirilly D, Xie T. Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development. 2007;134(6):1071–80. doi: 10.1242/dev.003392 17287246.

25. Williamson A, Lehmann R. Germ cell development in Drosophila. Annual review of cell and developmental biology. 1996;12:365–91. Epub 1996/01/01. doi: 10.1146/annurev.cellbio.12.1.365 8970731.

26. Godt D, Laski FA. Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric a brac. Development. 1995;121(1):173–87. Epub 1995/01/01. 7867498.

27. Li MA, Alls JD, Avancini RM, Koo K, Godt D. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nature cell biology. 2003;5(11):994–1000. Epub 2003/10/28. doi: 10.1038/ncb1058 14578908.

28. Asaoka M, Lin H. Germline stem cells in the Drosophila ovary descend from pole cells in the anterior region of the embryonic gonad. Development. 2004;131(20):5079–89. Epub 2004/10/02. doi: 10.1242/dev.01391 15459101.

29. Gilboa L. Organizing stem cell units in the Drosophila ovary. Curr Opin Genet Dev. 2015;32:31–6. Epub 2015/02/24. doi: 10.1016/j.gde.2015.01.005 25703842.

30. Chen J, Godt D, Gunsalus K, Kiss I, Goldberg M, Laski FA. Cofilin/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nature cell biology. 2001;3(2):204–9. doi: 10.1038/35055120 11175754.

31. Yatsenko AS, Shcherbata HR. Stereotypical architecture of the stem cell niche is spatiotemporally established by miR-125-dependent coordination of Notch and steroid signaling. Development. 2018;145(3). Epub 2018/01/24. doi: 10.1242/dev.159178 29361571; PubMed Central PMCID: PMC5818007.

32. Eliazer S, Buszczak M. Finding a niche: studies from the Drosophila ovary. Stem cell research & therapy. 2011;2(6):45. Epub 2011/11/29. doi: 10.1186/scrt86 22117545; PubMed Central PMCID: PMC3340554.

33. Panchal T, Chen X, Alchits E, Oh Y, Poon J, Kouptsova J, et al. Specification and spatial arrangement of cells in the germline stem cell niche of the Drosophila ovary depend on the Maf transcription factor Traffic jam. PLoS Genet. 2017;13(5):e1006790. Epub 2017/05/26. doi: 10.1371/journal.pgen.1006790 28542174; PubMed Central PMCID: PMC5459507.

34. Spradling AC, Nystul T, Lighthouse D, Morris L, Fox D, Cox R, et al. Stem cells and their niches: integrated units that maintain Drosophila tissues. Cold Spring Harb Symp Quant Biol. 2008;73:49–57. Epub 2008/11/22. sqb.2008.73.023 [pii] doi: 10.1101/sqb.2008.73.023 19022764.

35. Chen D, McKearin DM. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 2003;130(6):1159–70. Epub 2003/02/07. doi: 10.1242/dev.00325 12571107.

36. Xie T, Spradling AC. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell. 1998;94(2):251–60. Epub 1998/08/08. S0092-8674(00)81424-5 [pii]. doi: 10.1016/s0092-8674(00)81424-5 9695953.

37. Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, et al. Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development. 2004;131(6):1353–64. Epub 2004/02/20. doi: 10.1242/dev.01026 [pii]. 14973291.

38. Hsu HJ, Drummond-Barbosa D. Insulin signals control the competence of the Drosophila female germline stem cell niche to respond to Notch ligands. Developmental biology. 2011;350(2):290–300. Epub 2010/12/15. doi: 10.1016/j.ydbio.2010.11.032 21145317.

39. Shimizu H, Wilkin MB, Woodcock SA, Bonfini A, Hung Y, Mazaleyrat S, et al. The Drosophila ZO-1 protein Polychaetoid suppresses Deltex-regulated Notch activity to modulate germline stem cell niche formation. Open Biol. 2017;7(4). Epub 2017/04/21. doi: 10.1098/rsob.160322 28424321; PubMed Central PMCID: PMC5413905.

40. Langridge PD, Struhl G. Epsin-Dependent Ligand Endocytosis Activates Notch by Force. Cell. 2017;171(6):1383–96 e12. Epub 2017/12/02. doi: 10.1016/j.cell.2017.10.048 29195077.

41. Trylinski M, Mazouni K, Schweisguth F. Intra-lineage Fate Decisions Involve Activation of Notch Receptors Basal to the Midbody in Drosophila Sensory Organ Precursor Cells. Curr Biol. 2017;27(15):2239–47 e3. Epub 2017/07/25. doi: 10.1016/j.cub.2017.06.030 28736165.

42. Shcherbata HR, Althauser C, Findley SD, Ruohola-Baker H. The mitotic-to-endocycle switch in Drosophila follicle cells is executed by Notch-dependent regulation of G1/S, G2/M and M/G1 cell-cycle transitions. Development. 2004;131(13):3169–81. Epub 2004/06/04. doi: 10.1242/dev.01172 15175253.

43. de Celis JF, Tyler DM, de Celis J, Bray SJ. Notch signalling mediates segmentation of the Drosophila leg. Development. 1998;125(23):4617–26. 9806911.

44. Bolivar J, Pearson J, Lopez-Onieva L, Gonzalez-Reyes A. Genetic dissection of a stem cell niche: the case of the Drosophila ovary. Dev Dyn. 2006;235(11):2969–79. doi: 10.1002/dvdy.20967 17013875.

45. Matsuda M, Koga M, Woltjen K, Nishida E, Ebisuya M. Synthetic lateral inhibition governs cell-type bifurcation with robust ratios. Nat Commun. 2015;6:6195. doi: 10.1038/ncomms7195 25652697.

46. Gancz D, Gilboa L. Insulin and Target of rapamycin signaling orchestrate the development of ovarian niche-stem cell units in Drosophila. Development. 2013;140(20):4145–54. Epub 2013/09/13. doi: 10.1242/dev.093773 24026119.

47. Gancz D, Lengil T, Gilboa L. Coordinated regulation of niche and stem cell precursors by hormonal signaling. PLoS biology. 2011;9(11):e1001202. Epub 2011/12/02. doi: 10.1371/journal.pbio.1001202 22131903; PubMed Central PMCID: PMC3222635.

48. Sarikaya DP, Extavour CG. The Hippo pathway regulates homeostatic growth of stem cell niche precursors in the Drosophila ovary. PLoS Genet. 2015;11(2):e1004962. doi: 10.1371/journal.pgen.1004962 25643260.

49. Hodin J, Riddiford LM. The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev Genes Evol. 1998;208(6):304–17. doi: 10.1007/s004270050186 9716721.

50. Assa-Kunik E, Torres IL, Schejter ED, Johnston DS, Shilo BZ. Drosophila follicle cells are patterned by multiple levels of Notch signaling and antagonism between the Notch and JAK/STAT pathways. Development. 2007;134(6):1161–9. Epub 2007/03/03. doi: 10.1242/dev.02800 17332535.

51. Larkin MK, Holder K, Yost C, Giniger E, Ruohola-Baker H. Expression of constitutively active Notch arrests follicle cells at a precursor stage during Drosophila oogenesis and disrupts the anterior-posterior axis of the oocyte. Development. 1996;122(11):3639–50. Epub 1996/11/01. 8951079.

52. Wilcockson SG, Ashe HL. Drosophila Ovarian Germline Stem Cell Cytocensor Projections Dynamically Receive and Attenuate BMP Signaling. Dev Cell. 2019;50(3):296–312 e5. Epub 2019/06/11. doi: 10.1016/j.devcel.2019.05.020 31178401; PubMed Central PMCID: PMC6688100.

53. Nieuwburg R, Nashchekin D, Jakobs M, Carter AP, Khuc Trong P, Goldstein RE, et al. Localised dynactin protects growing microtubules to deliver oskar mRNA to the posterior cortex of the Drosophila oocyte. Elife. 2017;6. Epub 2017/10/17. doi: 10.7554/eLife.27237 29035202; PubMed Central PMCID: PMC5643094.

54. Rodriguez-Mesa E, Abreu-Blanco MT, Rosales-Nieves AE, Parkhurst SM. Developmental expression of Drosophila Wiskott-Aldrich Syndrome family proteins. Dev Dyn. 2012;241(3):608–26. Epub 2012/01/26. doi: 10.1002/dvdy.23742 22275148; PubMed Central PMCID: PMC3288701.

55. Roy S, Huang H, Liu S, Kornberg TB. Cytoneme-mediated contact-dependent transport of the Drosophila decapentaplegic signaling protein. Science. 2014;343(6173):1244624. Epub 2014/01/05. doi: 10.1126/science.1244624 24385607; PubMed Central PMCID: PMC4336149.

56. Ramirez-Weber FA, Kornberg TB. Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell. 1999;97(5):599–607. Epub 1999/06/15. doi: 10.1016/s0092-8674(00)80771-0 10367889.

57. Hsiung F, Ramirez-Weber FA, Iwaki DD, Kornberg TB. Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature. 2005;437(7058):560–3. Epub 2005/09/24. doi: 10.1038/nature03951 16177792.

58. Chen W, Huang H, Hatori R, Kornberg TB. Essential basal cytonemes take up Hedgehog in the Drosophila wing imaginal disc. Development. 2017;144(17):3134–44. Epub 2017/07/27. doi: 10.1242/dev.149856 28743798; PubMed Central PMCID: PMC5611956.

59. Fereres S, Hatori R, Hatori M, Kornberg TB. Cytoneme-mediated signaling essential for tumorigenesis. PLoS Genet. 2019;15(9):e1008415. Epub 2019/10/01. doi: 10.1371/journal.pgen.1008415 31568500; PubMed Central PMCID: PMC6786653.

60. Yamamoto S, Schulze KL, Bellen HJ. Introduction to Notch signaling. Methods Mol Biol. 2014;1187:1–14. Epub 2014/07/24. doi: 10.1007/978-1-4939-1139-4_1 25053477.

61. Perez-Mockus G, Schweisguth F. Cell Polarity and Notch Signaling: Linked by the E3 Ubiquitin Ligase Neuralized? Bioessays. 2017;39(11). Epub 2017/09/25. doi: 10.1002/bies.201700128 28940548.

62. Bischoff M, Gradilla AC, Seijo I, Andres G, Rodriguez-Navas C, Gonzalez-Mendez L, et al. Cytonemes are required for the establishment of a normal Hedgehog morphogen gradient in Drosophila epithelia. Nature cell biology. 2013;15(11):1269–81. doi: 10.1038/ncb2856 24121526; PubMed Central PMCID: PMC3840581.

63. Huang H, Kornberg TB. Cells must express components of the planar cell polarity system and extracellular matrix to support cytonemes. Elife. 2016;5. doi: 10.7554/eLife.18979 27591355; PubMed Central PMCID: PMC5030081.

64. Konig A, Shcherbata HR. Soma influences GSC progeny differentiation via the cell adhesion-mediated steroid-let-7-Wingless signaling cascade that regulates chromatin dynamics. Biol Open. 2015;4(3):285–300. Epub 2015/02/11. doi: 10.1242/bio.201410553 25661868; PubMed Central PMCID: PMC4359735.

65. Rojas-Rios P, Guerrero I, Gonzalez-Reyes A. Cytoneme-mediated delivery of hedgehog regulates the expression of bone morphogenetic proteins to maintain germline stem cells in Drosophila. PLoS biology. 2012;10(4):e1001298. Epub 2012/04/18. doi: 10.1371/journal.pbio.1001298 22509132; PubMed Central PMCID: PMC3317903.

66. Inaba M, Buszczak M, Yamashita YM. Nanotubes mediate niche-stem-cell signalling in the Drosophila testis. Nature. 2015;523(7560):329–32. Epub 2015/07/02. doi: 10.1038/nature14602 26131929; PubMed Central PMCID: PMC4586072.

67. Roy S, Hsiung F, Kornberg TB. Specificity of Drosophila cytonemes for distinct signaling pathways. Science. 2011;332(6027):354–8. Epub 2011/04/16. doi: 10.1126/science.1198949 21493861; PubMed Central PMCID: PMC3109072.

68. Kornberg TB. Cytonemes extend their reach. EMBO J. 2013;32(12):1658–9. Epub 2013/05/16. doi: 10.1038/emboj.2013.115 23673359; PubMed Central PMCID: PMC3680737.

69. Kornberg TB. Distributing signaling proteins in space and time: the province of cytonemes. Curr Opin Genet Dev. 2017;45:22–7. Epub 2017/03/01. doi: 10.1016/j.gde.2017.02.010 28242479; PubMed Central PMCID: PMC5502195.

70. Couderc JL, Godt D, Zollman S, Chen J, Li M, Tiong S, et al. The bric a brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development. 2002;129(10):2419–33. Epub 2002/04/26. 11973274.

71. Heitzler P, Simpson P. The choice of cell fate in the epidermis of Drosophila. Cell. 1991;64(6):1083–92. Epub 1991/03/22. doi: 10.1016/0092-8674(91)90263-x 2004417.

72. Konig A, Shcherbata HR. Visualization of adult stem cells within their niches using the Drosophila germline as a model system. Methods Mol Biol. 2013;1035:25–33. Epub 2013/08/21. doi: 10.1007/978-1-62703-508-8_3 23959979.


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