Characterization of centriole duplication in human epidermis, Bowen's disease, and squamous cell carcinoma

Saori Watanuki, Harumi Fujita, Keisuke Koyama, Masayuki Amagai, Akiharu Kubo

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Abstract

Background: Centrosomes contain two centrioles: a pre-existing mature centriole and a newly formed immature centriole. Each centriole is duplicated once within a cell cycle, which is crucial for proper centrosome duplication and cell division. Objective: To describe the centrosome duplication cycle in human epidermis, Bowen's disease (BD), and squamous cell carcinoma (SCC). Methods: Immunofluorescent staining of centriolar proteins and Ki-67 was used to evaluate cell cycles and the number of centrioles. Centrobin and Outer dense fiber of sperm tails 2 (ODF2) were used as markers for immature and mature centrioles, respectively. Results: Normal human primary epidermal keratinocytes in a monolayered culture have one centrobin+ centriole (CTRB1+ cells) supposed in G0/G1 phases or have two centrobin+ centrioles (CTRB2+ cells) supposed in S−G2 phase. In a three-dimensional culture and in vivo human epidermis, the majority of suprabasal cells were CTRB2+ cells, in spite of their non-proliferative Ki-67 nature. The tumor mass of BD and SCC contained CTRB1+ cells and Ki-67+ proliferating and Ki-67 non-proliferative CTRB2+ cells. Clumping cells in BD had increased numbers of centrioles, with an approximate 1:1 to 2:1 ratio of centrobin+ to ODF2+ centrioles. Conclusions: The cell cycle arrest of suprabasal cells is distinct from the G0 arrest of monolayered epithelial cells. Tumor mass of BD and SCC contained non-proliferative cells with the characteristics of the suprabasal cells of normal epidermis. A constant ratio of the number of centrobin+ to ODF2+ centrioles indicates that multiple centrioles were induced by cell division failure rather than centriole overduplication in clumping cells.

Original languageEnglish
JournalJournal of Dermatological Science
DOIs
Publication statusAccepted/In press - 2018 Jan 1

Fingerprint

Bowen's Disease
Centrioles
Epidermis
Squamous Cell Carcinoma
Cells
Fibers
Tumors
Sperm Tail
Centrosome
Cell Division
Epithelial Cells
Cell Cycle
Cell Cycle Resting Phase
G1 Phase
Proteins
Cell Cycle Checkpoints
Keratinocytes

Keywords

  • Bowen's disease
  • Cell cycle
  • Centriole
  • Centrosome
  • Clumping cells

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Dermatology

Cite this

@article{cbd31a12c94b49fc93c24ffcf06aecc4,
title = "Characterization of centriole duplication in human epidermis, Bowen's disease, and squamous cell carcinoma",
abstract = "Background: Centrosomes contain two centrioles: a pre-existing mature centriole and a newly formed immature centriole. Each centriole is duplicated once within a cell cycle, which is crucial for proper centrosome duplication and cell division. Objective: To describe the centrosome duplication cycle in human epidermis, Bowen's disease (BD), and squamous cell carcinoma (SCC). Methods: Immunofluorescent staining of centriolar proteins and Ki-67 was used to evaluate cell cycles and the number of centrioles. Centrobin and Outer dense fiber of sperm tails 2 (ODF2) were used as markers for immature and mature centrioles, respectively. Results: Normal human primary epidermal keratinocytes in a monolayered culture have one centrobin+ centriole (CTRB1+ cells) supposed in G0/G1 phases or have two centrobin+ centrioles (CTRB2+ cells) supposed in S−G2 phase. In a three-dimensional culture and in vivo human epidermis, the majority of suprabasal cells were CTRB2+ cells, in spite of their non-proliferative Ki-67− nature. The tumor mass of BD and SCC contained CTRB1+ cells and Ki-67+ proliferating and Ki-67− non-proliferative CTRB2+ cells. Clumping cells in BD had increased numbers of centrioles, with an approximate 1:1 to 2:1 ratio of centrobin+ to ODF2+ centrioles. Conclusions: The cell cycle arrest of suprabasal cells is distinct from the G0 arrest of monolayered epithelial cells. Tumor mass of BD and SCC contained non-proliferative cells with the characteristics of the suprabasal cells of normal epidermis. A constant ratio of the number of centrobin+ to ODF2+ centrioles indicates that multiple centrioles were induced by cell division failure rather than centriole overduplication in clumping cells.",
keywords = "Bowen's disease, Cell cycle, Centriole, Centrosome, Clumping cells",
author = "Saori Watanuki and Harumi Fujita and Keisuke Koyama and Masayuki Amagai and Akiharu Kubo",
year = "2018",
month = "1",
day = "1",
doi = "10.1016/j.jdermsci.2018.03.008",
language = "English",
journal = "Journal of Dermatological Science",
issn = "0923-1811",
publisher = "Elsevier Ireland Ltd",

}

TY - JOUR

T1 - Characterization of centriole duplication in human epidermis, Bowen's disease, and squamous cell carcinoma

AU - Watanuki, Saori

AU - Fujita, Harumi

AU - Koyama, Keisuke

AU - Amagai, Masayuki

AU - Kubo, Akiharu

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Background: Centrosomes contain two centrioles: a pre-existing mature centriole and a newly formed immature centriole. Each centriole is duplicated once within a cell cycle, which is crucial for proper centrosome duplication and cell division. Objective: To describe the centrosome duplication cycle in human epidermis, Bowen's disease (BD), and squamous cell carcinoma (SCC). Methods: Immunofluorescent staining of centriolar proteins and Ki-67 was used to evaluate cell cycles and the number of centrioles. Centrobin and Outer dense fiber of sperm tails 2 (ODF2) were used as markers for immature and mature centrioles, respectively. Results: Normal human primary epidermal keratinocytes in a monolayered culture have one centrobin+ centriole (CTRB1+ cells) supposed in G0/G1 phases or have two centrobin+ centrioles (CTRB2+ cells) supposed in S−G2 phase. In a three-dimensional culture and in vivo human epidermis, the majority of suprabasal cells were CTRB2+ cells, in spite of their non-proliferative Ki-67− nature. The tumor mass of BD and SCC contained CTRB1+ cells and Ki-67+ proliferating and Ki-67− non-proliferative CTRB2+ cells. Clumping cells in BD had increased numbers of centrioles, with an approximate 1:1 to 2:1 ratio of centrobin+ to ODF2+ centrioles. Conclusions: The cell cycle arrest of suprabasal cells is distinct from the G0 arrest of monolayered epithelial cells. Tumor mass of BD and SCC contained non-proliferative cells with the characteristics of the suprabasal cells of normal epidermis. A constant ratio of the number of centrobin+ to ODF2+ centrioles indicates that multiple centrioles were induced by cell division failure rather than centriole overduplication in clumping cells.

AB - Background: Centrosomes contain two centrioles: a pre-existing mature centriole and a newly formed immature centriole. Each centriole is duplicated once within a cell cycle, which is crucial for proper centrosome duplication and cell division. Objective: To describe the centrosome duplication cycle in human epidermis, Bowen's disease (BD), and squamous cell carcinoma (SCC). Methods: Immunofluorescent staining of centriolar proteins and Ki-67 was used to evaluate cell cycles and the number of centrioles. Centrobin and Outer dense fiber of sperm tails 2 (ODF2) were used as markers for immature and mature centrioles, respectively. Results: Normal human primary epidermal keratinocytes in a monolayered culture have one centrobin+ centriole (CTRB1+ cells) supposed in G0/G1 phases or have two centrobin+ centrioles (CTRB2+ cells) supposed in S−G2 phase. In a three-dimensional culture and in vivo human epidermis, the majority of suprabasal cells were CTRB2+ cells, in spite of their non-proliferative Ki-67− nature. The tumor mass of BD and SCC contained CTRB1+ cells and Ki-67+ proliferating and Ki-67− non-proliferative CTRB2+ cells. Clumping cells in BD had increased numbers of centrioles, with an approximate 1:1 to 2:1 ratio of centrobin+ to ODF2+ centrioles. Conclusions: The cell cycle arrest of suprabasal cells is distinct from the G0 arrest of monolayered epithelial cells. Tumor mass of BD and SCC contained non-proliferative cells with the characteristics of the suprabasal cells of normal epidermis. A constant ratio of the number of centrobin+ to ODF2+ centrioles indicates that multiple centrioles were induced by cell division failure rather than centriole overduplication in clumping cells.

KW - Bowen's disease

KW - Cell cycle

KW - Centriole

KW - Centrosome

KW - Clumping cells

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