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Over-expression of Plk4 induces centrosome amplification, loss of primary cilia and associated tissue hyperplasia in the mouse

Over-expression of Plk4 induces centrosome amplification, loss of primary cilia and associated tissue hyperplasia in the mouse
Over-expression of Plk4 induces centrosome amplification, loss of primary cilia and associated tissue hyperplasia in the mouse

To address the long-known relationship between supernumerary centrosomes and cancer, we have generated a transgenic mouse that permits inducible expression of the master regulator of centriole duplication, Polo-like-kinase-4 (Plk4). Over-expression of Plk4 from this transgene advances the onset of tumour formation that occurs in the absence of the tumour suppressor p53. Plk4 over-expression also leads to hyperproliferation of cells in the pancreas and skin that is enhanced in a p53 null background. Pancreatic islets become enlarged following Plk4 over-expression as a result of equal expansion of α- and β-cells, which exhibit centrosome amplification. Mice overexpressing Plk4 develop grey hair due to a loss of differentiated melanocytes and bald patches of skin associated with a thickening of the epidermis. This reflects an increase in proliferating cells expressing keratin 5 in the basal epidermal layer and the expansion of these cells into suprabasal layers. Such cells also express keratin 6, a marker for hyperplasia. This is paralleled by a decreased expression of later differentiation markers, involucrin, filaggrin and loricrin. Proliferating cells showed an increase in centrosome number and a loss of primary cilia, events that were mirrored in primary cultures of keratinocytes established from these animals. We discuss how repeated duplication of centrioles appears to prevent the formation of basal bodies leading to loss of primary cilia, disruption of signalling and thereby aberrant differentiation of cells within the epidermis. The absence of p53 permits cells with increased centrosomes to continue dividing, thus setting up a neoplastic state of error prone mitoses, a prerequisite for cancer development.

Animals, Cell Proliferation, Cells, Cultured, Centrioles/metabolism, Centrosome/metabolism, Cilia/metabolism, Filaggrin Proteins, Hyperplasia/metabolism, Intermediate Filament Proteins/metabolism, Islets of Langerhans/metabolism, Membrane Proteins/metabolism, Mice, Protein Precursors/metabolism, Protein Serine-Threonine Kinases/genetics
150209
Coelho, Paula A.
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Bury, Leah
587c6158-be55-4dec-9aa9-7bf08b788362
Shahbazi, Marta N.
17e424b6-4c4d-4b0e-9efc-4d1b1ac82029
Liakath-Ali, Kifayathullah
8d5a020c-e976-4901-9195-68f4bc0de74e
Tate, Peri H.
99bab23a-5545-4686-b3a1-d40d0916b73a
Wormald, Sam
4936e04e-7850-4bd7-a02c-ae19f2fd6055
Hindley, Christopher J.
3f009c77-55b7-4810-b741-6a67618e1406
Huch, Meritxell
defdc21f-6ca2-4a97-ab38-436adce9d37c
Archer, Joy
d98afeb8-a5e0-45b7-8737-ae38ec7914f5
Skarnes, William C.
cedd85cf-a7c9-477b-8809-28e8de634282
Zernicka-Goetz, Magdalena
23e25dfb-8cf4-4a17-b555-cc7b9d072f20
Glover, David M.
c64b6b81-5c2b-4e63-9088-875f9a18d169
Coelho, Paula A.
2b828555-57a4-4a02-905c-75080ee55c45
Bury, Leah
587c6158-be55-4dec-9aa9-7bf08b788362
Shahbazi, Marta N.
17e424b6-4c4d-4b0e-9efc-4d1b1ac82029
Liakath-Ali, Kifayathullah
8d5a020c-e976-4901-9195-68f4bc0de74e
Tate, Peri H.
99bab23a-5545-4686-b3a1-d40d0916b73a
Wormald, Sam
4936e04e-7850-4bd7-a02c-ae19f2fd6055
Hindley, Christopher J.
3f009c77-55b7-4810-b741-6a67618e1406
Huch, Meritxell
defdc21f-6ca2-4a97-ab38-436adce9d37c
Archer, Joy
d98afeb8-a5e0-45b7-8737-ae38ec7914f5
Skarnes, William C.
cedd85cf-a7c9-477b-8809-28e8de634282
Zernicka-Goetz, Magdalena
23e25dfb-8cf4-4a17-b555-cc7b9d072f20
Glover, David M.
c64b6b81-5c2b-4e63-9088-875f9a18d169

Coelho, Paula A., Bury, Leah, Shahbazi, Marta N., Liakath-Ali, Kifayathullah, Tate, Peri H., Wormald, Sam, Hindley, Christopher J., Huch, Meritxell, Archer, Joy, Skarnes, William C., Zernicka-Goetz, Magdalena and Glover, David M. (2015) Over-expression of Plk4 induces centrosome amplification, loss of primary cilia and associated tissue hyperplasia in the mouse. Open Biology, 5 (12), 150209. (doi:10.1098/rsob.150209).

Record type: Article

Abstract

To address the long-known relationship between supernumerary centrosomes and cancer, we have generated a transgenic mouse that permits inducible expression of the master regulator of centriole duplication, Polo-like-kinase-4 (Plk4). Over-expression of Plk4 from this transgene advances the onset of tumour formation that occurs in the absence of the tumour suppressor p53. Plk4 over-expression also leads to hyperproliferation of cells in the pancreas and skin that is enhanced in a p53 null background. Pancreatic islets become enlarged following Plk4 over-expression as a result of equal expansion of α- and β-cells, which exhibit centrosome amplification. Mice overexpressing Plk4 develop grey hair due to a loss of differentiated melanocytes and bald patches of skin associated with a thickening of the epidermis. This reflects an increase in proliferating cells expressing keratin 5 in the basal epidermal layer and the expansion of these cells into suprabasal layers. Such cells also express keratin 6, a marker for hyperplasia. This is paralleled by a decreased expression of later differentiation markers, involucrin, filaggrin and loricrin. Proliferating cells showed an increase in centrosome number and a loss of primary cilia, events that were mirrored in primary cultures of keratinocytes established from these animals. We discuss how repeated duplication of centrioles appears to prevent the formation of basal bodies leading to loss of primary cilia, disruption of signalling and thereby aberrant differentiation of cells within the epidermis. The absence of p53 permits cells with increased centrosomes to continue dividing, thus setting up a neoplastic state of error prone mitoses, a prerequisite for cancer development.

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coelho-et-al-2015-over-expression-of-plk4-induces-centrosome-amplification-loss-of-primary-cilia-and-associated-tissue - Version of Record
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Published date: 1 December 2015
Keywords: Animals, Cell Proliferation, Cells, Cultured, Centrioles/metabolism, Centrosome/metabolism, Cilia/metabolism, Filaggrin Proteins, Hyperplasia/metabolism, Intermediate Filament Proteins/metabolism, Islets of Langerhans/metabolism, Membrane Proteins/metabolism, Mice, Protein Precursors/metabolism, Protein Serine-Threonine Kinases/genetics

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Local EPrints ID: 491317
URI: http://eprints.soton.ac.uk/id/eprint/491317
PURE UUID: bbb2cbf0-82cd-4408-b222-ba987b5b4fca
ORCID for Kifayathullah Liakath-Ali: ORCID iD orcid.org/0000-0001-9047-7424

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Date deposited: 19 Jun 2024 16:52
Last modified: 20 Jun 2024 02:06

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Contributors

Author: Paula A. Coelho
Author: Leah Bury
Author: Marta N. Shahbazi
Author: Kifayathullah Liakath-Ali ORCID iD
Author: Peri H. Tate
Author: Sam Wormald
Author: Christopher J. Hindley
Author: Meritxell Huch
Author: Joy Archer
Author: William C. Skarnes
Author: Magdalena Zernicka-Goetz
Author: David M. Glover

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