Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 348

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila

Kango-Singh, Madhuri, Nolo, Riitta, Tao, Chunyao, Verstreken, Patrik, Hiesinger, P. Robin, Bellen, Hugo J., Halder, Georg·2002·Development

Abstract

During animal development, organ size is determined primarily by the amount of cell proliferation, which must be tightly regulated to ensure the generation of properly proportioned organs. However, little is known about the molecular pathways that direct cells to stop proliferating when an organ has attained its proper size. We have identified mutations in a novel gene,shar-pei, that is required for proper termination of cell proliferation during Drosophila imaginal disc development. Clones ofshar-pei mutant cells in imaginal discs produce enlarged tissues containing more cells of normal size. We show that this phenotype is the result of both increased cell proliferation and reduced apoptosis. Hence,shar-pei restricts cell proliferation and promotes apoptosis. By contrast, shar-pei is not required for cell differentiation and pattern formation of adult tissue. Shar-pei is also not required for cell cycle exit during terminal differentiation, indicating that the mechanisms directing cell proliferation arrest during organ growth are distinct from those directing cell cycle exit during terminal differentiation.shar-pei encodes a WW-domain-containing protein that has homologs in worms, mice and humans, suggesting that mechanisms of organ growth control are evolutionarily conserved.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1242/dev.00168

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 81

  1. Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A.,Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A.,Galle, R. F. et al. (2000). The genome sequence of Drosophila melanogaster. Science287,2185-2195. · DOI · Paper page
  2. Agrawal, N., Kango, M., Mishra, A. and Sinha, P.(1995). Neoplastic transformation and aberrant cell-cell interactions in genetic mosaics of lethal(2)giant larvae (lgl), a tumor suppressor gene of Drosophila. Dev. Biol.172,218-229. · DOI
  3. Asano, M., Nevins, J. R. and Wharton, R. P.(1996). Ectopic E2F expression induces S phase and apoptosis in Drosophila imaginal discs. Genes Dev.10,1422-1432. · DOI
  4. Baker, N. E. (2001). Cell proliferation,survival, and death in the Drosophila eye. Semin. Cell Dev. Biol.12,499-507. · DOI
  5. Bilder, D., Li, M. and Perrimon, N. (2000). Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science289,113-116. · DOI · Paper page
  6. Braet, F., de Zanger, R. and Wisse, E. (1997). Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells. J. Microsc.186, 84-87. · DOI · Paper page
  7. Bryant P. J. (1978). Pattern formation in the imaginal discs. In Genetics and Biology of Drosophila,Vol. 2c (ed. M. Ashburner and T. R. F. Wright), pp.337-358. New York: Academic Press.
  8. Bryant P. J. (1987). Experimental and genetic analysis of growth and cell proliferation in Drosophila imaginal discs. In Genetic Regulation of Development (ed. W. Loomis), pp. 339-372. New York: Alan R. Liss.
  9. Bryant, P. J. and Levinson, P. (1985). Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. Dev. Biol.107,355-363. · DOI · Paper page
  10. Bryant, P. J. and Simpson, P. (1984). Intrinsic and extrinsic control of growth in developing organs. Q. Rev. Biol.59,387-415. · DOI · Paper page
  11. Bryant, P. J., Huettner, B., Held, L. I., Jr, Ryerse, J. and Szidonya, J. (1988). Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila.Dev. Biol.129,541-554. · DOI · Paper page
  12. Butler, S. J., Ray, S. and Hiromi, Y. (1997). klingon, a novel member of the Drosophila immunoglobulin superfamily, is required for the development of the R7 photoreceptor neuron.Development124,781-792. · DOI
  13. Cho, K. O., Chern, J., Izaddoost, S. and Choi, K. W.(2000). Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell103,331-342. · DOI
  14. Cohen, S. M. (1993). Imaginal disc development. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 747-781. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
  15. Crack, D., Secombe, J., Coombe, M., Brumby, A., Saint, R. and Richardson, H. (2002). Analysis of Drosophila cyclin EI and II function during development: identification of an inhibitory zone within the morphogenetic furrow of the eye imaginal disc that blocks the function of cyclin EI but not cyclin EII. Dev. Biol.241,157-171. · DOI
  16. Datar, S. A., Jacobs, H. W., de la Cruz, A. F., Lehner, C. F. and Edgar, B. A. (2000). The Drosophila cyclin D-Cdk4 complex promotes cellular growth. EMBO J.19,4543-4554. · DOI · Paper page
  17. Day, S. J. and Lawrence, P. A. (2000). Measuring dimensions: the regulation of size and shape.Development127,2977-2987. · DOI · Paper page
  18. de Nooij, J. C., Letendre, M. A. and Hariharan, I. K.(1996). A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis.Cell87,1237-1247. · DOI · Paper page
  19. Dickson, B. and Hafen, E. (1993). Genetic dissection of eye development in Drosophila. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp 1327-1362. Cold Spring Harbor,NY: Cold Spring Harbor Laboratory Press.
  20. Du, W. and Dyson, N. (1999). The role of RBF in the introduction of G1 regulation during Drosophila embryogenesis.EMBO J.18,916-925. · doi:10.1093/emboj/18.4.916
  21. Du, W., Vidal, M., Xie, J. E. and Dyson, N.(1996a). RBF, a novel RB-related gene that regulates E2F activity and interacts with cyclin E in Drosophila. Genes Dev.10,1206-1218. · DOI · Paper page
  22. Du, W., Xie, J. E. and Dyson, N. (1996b). Ectopic expression of dE2F and dDP induces cell proliferation and death in the Drosophila eye. EMBO J.15,3684-3692. · DOI
  23. Duman-Scheel, M., Weng, L., Xin, S. and Du, W.(2002). Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature417,299-304. · DOI · Paper page
  24. Edgar, B. A. and Lehner, C. F. (1996). Developmental control of cell cycle regulators: a fly's perspective.Science274,1646-1652. · DOI · Paper page
  25. Frankfort, B. J., Nolo, R., Zhang, Z., Bellen, H. J. and Mardon,G. (2001). senseless repression of rough is required for R8 photoreceptor differentiation in the developing Drosophila eye.Neuron32,403-414. · DOI
  26. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye.Cell87,651-660. · DOI · Paper page
  27. French, V., Bryant, P. J. and Bryant, S. V.(1976). Pattern regulation in epimorphic fields.Science193,969-981. · DOI · Paper page
  28. Garcia-Bellido, A. (1965). Larvalentwicklung transplantierter Organe von Drosophila melanogaster im Adultmilieu.J. Insect Physiol.11,1071-1078. · DOI
  29. Garoia, F., Guerra, D., Pezzoli, M. C., Lopez-Varea, A.,Cavicchi, S. and Garcia-Bellido, A. (2000). Cell behaviour of Drosophila fat cadherin mutations in wing development. Mech. Dev.94,95-109. · DOI
  30. Halder, G., Callaerts, P., Flister, S., Walldorf, U., Kloter, U. and Gehring, W. J. (1998). Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development125,2181-2191. · DOI · Paper page
  31. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila.Development120,2121-2129. · DOI · Paper page
  32. Haynie, J. L. and Bryant, P. J. (1977). The effects of X-rays on the proliferation dynamics of cells in the imaginal wing disc of Drosophila melanogaster. Roux Arch. Dev. Biol.183,85-100. · DOI · Paper page
  33. Johnston, L. A. and Gallant, P. (2002). Control of growth and organ size in Drosophila. BioEssays24, 54-64. · DOI · Paper page
  34. Kirby, B. S. and Bryant, P. J. (1982). Growth is required for cell competition in the imaginal discs of Drosophila melanogaster. Roux Arch. Dev. Biol.191,289-291. · doi:10.1007/bf00848419
  35. Knoblich, J. A., Sauer, K., Jones, L., Richardson, H., Saint, R. and Lehner, C. F. (1994). Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell77,107-120. · DOI · Paper page
  36. Kumar, J. P. and Moses, K. (2000). Cell fate specification in the Drosophila retina. Results Probl. Cell Differ.31,93-114. · DOI
  37. Lane, M. E., Sauer, K., Wallace, K., Jan, Y. N., Lehner, C. F. and Vaessin, H. (1996). Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development.Cell87,1225-1235. · DOI · Paper page
  38. Lawrence, P. A. and Struhl, G. (1996). Morphogens, compartments, and pattern: Lessons from Drosophila?Cell85,951-961. · DOI · Paper page
  39. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron22,451-461. · DOI · Paper page
  40. Lehman, D. A., Patterson, B., Johnston, L. A., Balzer, T.,Britton, J. S., Saint, R. and Edgar, B. A. (1999). Cis-regulatory elements of the mitotic regulator, string/Cdc25.Development126,1793-1803. · DOI
  41. Liu, T. H., Li, L. and Vaessin, H. (2002). Transcription of the Drosophila CKI gene dacapo is regulated by a modular array of cis-regulatory sequences. Mech. Dev.112, 25-36. · DOI
  42. Lo, P. C. and Frasch, M. (1997). A novel KH-domain protein mediates cell adhesion processes in Drosophila.Dev. Biol.190,241-256. · doi:10.1006/dbio.1997.8699
  43. Macias, M. J., Wiesner, S. and Sudol, M.(2002). WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett.513, 30-37. · DOI · Paper page
  44. Mahoney, P. A., Weber, U., Onofrechuk, P., Biessmann, H.,Bryant, P. J. and Goodman, C. S. (1991). The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell67,853-868. · DOI · Paper page
  45. Mansfield, E., Hersperger, E., Biggs, J. and Shearn, A.(1994). Genetic and molecular analysis of hyperplastic discs, a gene whose product is required for regulation of cell proliferation in Drosophila melanogaster imaginal discs and germ cells. Dev. Biol.165,507-526. · DOI
  46. Martin, P., Martin, A. and Shearn, A. (1977). Studies of l(3)c43hs1 a polyphasic, temperature-sensitive mutant of Drosophila melanogaster with a variety of imaginal disc defects. Dev. Biol.55,213-232. · doi:10.1016/0012-1606(77)90168-3
  47. Milan, M., Campuzano, S. and Garcia-Bellido, A.(1997). Developmental parameters of cell death in the wing disc of Drosophila. Proc. Natl. Acad. Sci. USA94,5691-5696. · DOI · Paper page
  48. Moberg, K. H., Bell, D. W., Wahrer, D. C., Haber, D. A. and Hariharan, I. K. (2001). Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines.Nature413,311-316. · DOI · Paper page
  49. Mohler, J. and Vani, K. (1992). Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila.Development115,957-971. · DOI · Paper page
  50. Morata, G. and Ripoll, P. (1975). Minutes:mutants of drosophila autonomously affecting cell division rate.Dev. Biol.42,211-221. · DOI · Paper page
  51. Neufeld, T. P., de la Cruz, A. F., Johnston, L. A. and Edgar, B. A. (1998). Coordination of growth and cell division in the Drosophila wing. Cell93,1183-1193. · DOI · Paper page
  52. Newsome, T. P., Asling, B. and Dickson, B. J.(2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development127,851-860. · DOI · Paper page
  53. Nolo, R., Abbott, L. A. and Bellen, H. J.(2000). Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila.Cell102,349-362. · DOI · Paper page
  54. O'Brochta, D. A. and Bryant, P. J. (1985). A zone of non-proliferating cells at a lineage restriction boundary in Drosophila. Nature313,138-141. · DOI
  55. O'Neill, E. M., Rebay, I., Tjian, R. and Rubin, G. M.(1994). The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway.Cell78,137-147. · DOI · Paper page
  56. Postlethwait, J. H. (1978). Clonal analysis ofDrosophila cuticular patterns. In Genetics and Biology of Drosophila, Vol. 2c (ed. M. Ashburner and T. R. F. Wright), pp. 359-441. New York: Academic Press.
  57. Potter, C. J. and Xu, T. (2001). Mechanisms of size control. Curr. Opin. Genet. Dev.11,279-286. · DOI
  58. Prober, D. A. and Edgar, B. A. (2001). Growth regulation by oncogenes—new insights from model organisms.Curr. Opin. Genet. Dev.11, 19-26. · DOI
  59. Reuter, G., Dorn, R., Wustmann, G., Friede, B. and Rauh, G.(1986). Third chromosome suppressor of position-effect variegation loci in Drosophila melanogaster. Mol. Gen. Genet.202,481-487. · DOI
  60. Richardson, H., O'Keefe, L. V., Marty, T. and Saint, R.(1995). Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc.Development121,3371-3379. · DOI · Paper page
  61. Richardson, H. E., O'Keefe, L. V., Reed, S. I. and Saint, R.(1993). A Drosophila G1-specific cyclin E homolog exhibits different modes of expression during embryogenesis.Development119,673-690. · DOI
  62. Robinow, S. and White, K. (1988). The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol.126,294-303. · DOI · Paper page
  63. Rusconi, J. C., Hays, R. and Cagan, R. L.(2000). Programmed cell death and patterning in Drosophila.Cell Death Differ.7,1063-1070. · DOI
  64. Serrano, N. and O'Farrell, P. H. (1997). Limb morphogenesis: connections between patterning and growth. Curr. Biol.7,R186-R195. · DOI
  65. Simpson, P. and Morata, G. (1981). Differential mitotic rates and patterns of growth in compartments in the Drosophila wing.Dev. Biol.85,299-308. · DOI · Paper page
  66. Spradling, A. C., Stern, D., Beaton, A., Rhem, E. J., Laverty,T., Mozden, N., Misra, S. and Rubin, G. M. (1999). The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes.Genetics153,135-177. · DOI · Paper page
  67. Stocker, H. and Hafen, E. (2000). Genetic control of cell size. Curr. Opin. Genet. Dev.10,529-535. · DOI · Paper page
  68. Tao, W., Zhang, S., Turenchalk, G. S., Stewart, R. A., St John,M. A., Chen, W. and Xu, T. (1999). Human homologue of the Drosophila melanogaster lats tumour suppressor modulates CDC2 activity.Nat. Genet.21,177-181. · DOI · Paper page
  69. Tapon, N., Moberg, K. H. and Hariharan, I. K.(2001). The coupling of cell growth to the cell cycle.Curr. Opin. Cell Biol.13,731-737. · DOI
  70. Turenchalk, G. S., St John, M. A., Tao, W. and Xu, T.(1999). The role of lats in cell cycle regulation and tumorigenesis. Biochim. Biophys. Acta1424,M9-M16. · DOI
  71. Valverde, P. (2000). Cloning, expression, and mapping of hWW45, a novel human WW domain- containing gene.Biochem. Biophys. Res. Commun.276,990-998. · DOI
  72. Watson, K. L., Justice, R. W. and Bryant, P. J.(1994). Drosophila in cancer research: the first fifty tumor suppressor genes. J. Cell Sci.18 Suppl., 19-33. · DOI
  73. Weinkove, D. and Leevers, S. J. (2000). The genetic control of organ growth: insights from Drosophila. Curr. Opin. Genet. Dev.10,75-80. · DOI
  74. Wolff, T. and Ready, D. F. (1991). Cell death in normal and rough eye mutants of Drosophila.Development113,825-839. · DOI · Paper page
  75. Wolff, T. and Ready, D. F. (1993). Pattern formation in Drosophila retina. In The Development ofDrosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp.1277-1325. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
  76. Woods, D. F. and Bryant, P. J. (1989). Molecular cloning of the lethal(1)discs large-1 oncogene of Drosophila.Dev. Biol.134,222-235. · DOI · Paper page
  77. Woods, D. F. and Bryant, P. J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell66,451-464. · DOI · Paper page
  78. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues.Development117,1223-1237. · DOI · Paper page
  79. Xu, T., Wang, W., Zhang, S., Stewart, R. A. and Yu, W.(1995). Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase.Development121,1053-1063. · DOI · Paper page
  80. Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L.,Feldman, R. M., Clem, R. J., Muller, H. A. and Hay, B. A.(2002). Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol.4, 416-424. · DOI · Paper page
  81. Zilian, O., Frei, E., Burke, R., Brentrup, D., Gutjahr, T.,Bryant, P. J. and Noll, M. (1999). double-time is identical to discs overgrown, which is required for cell survival, proliferation and growth arrest in Drosophila imaginal discs.Development126,5409-5420. · DOI

Cited by

See all 348

Metadata

Authors
Kango-Singh, M., Nolo, R., Tao, C., Verstreken, P., Hiesinger, P. R., Bellen, H. J., & Halder, G.
Venue
Development
Published
2002-12-15
Volume
129
Issue
24
Pages
5719-5730
ISSN
  • 0950-1991 (ISSN-L)
  • 1477-9129
OpenAlex
W2106029142
Cited by
348
References
4
FWCI
3.56
Type
journal article
Language
en
Open access
closed

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.