Holocrine glands

Holocrine Secretion Occurs outside the Tight Junction Barrier in Multicellular Glands: Lessons from Claudin-1-Deficient Mice

Holocrine secretion is a specific mode of secretion involving secretion of entire cytoplasmic materials with remnants of dead cells, as observed in multicellular exocrine glands of reptiles, birds, and mammals. Here, we found that sebaceous glands in mice, representative of multicellular exocrine glands of mammals, exhibit a form of polarized stratified epithelium equipped with tight junctions (TJs), and found that holocrine secretion occurred outside the TJ barriers. Sebaceous glands share characteristics of stratified epithelia with interfollicular epidermis, including basal-layer-restricted cell proliferation, TJ barrier formation at a specific single layer of cells with apico-basolateral plasma membrane polarity, and cell death outside the TJ barrier. Knockout of claudin-1, a transmembrane adhesive protein in TJs, in mice caused leakage of the TJ barrier in sebaceous glands and incomplete degradation of the plasma membrane and nuclei during holocrine secretion. Claudin-1 knockout resulted in the accumulation of incompletely degenerated sebocytes in sebaceous ducts, suggesting that the TJ barrier was necessary for differentiation of holocrine secretion. The redefinition of sebaceous glands as TJ-forming stratified epithelia provides an important framework to understand the molecular mechanism of holocrine secretion.

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Similar articles

Langbein L, Grund C, Kuhn C, Praetzel S, Kartenbeck J, Brandner JM, Moll I, Franke WW. Langbein L, et al. Eur J Cell Biol. 2002 Aug;81(8):419-35. doi: 10.1078/0171-9335-00270. Eur J Cell Biol. 2002. PMID: 12234014

Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Furuse M, et al. J Cell Biol. 2002 Mar 18;156(6):1099-111. doi: 10.1083/jcb.200110122. Epub 2002 Mar 11. J Cell Biol. 2002. PMID: 11889141 Free PMC article.

Otani T, Nguyen TP, Tokuda S, Sugihara K, Sugawara T, Furuse K, Miura T, Ebnet K, Furuse M. Otani T, et al. J Cell Biol. 2019 Oct 7;218(10):3372-3396. doi: 10.1083/jcb.201812157. Epub 2019 Aug 29. J Cell Biol. 2019. PMID: 31467165 Free PMC article.

Tsukita S, Furuse M. Tsukita S, et al. Genes Cells. 1998 Sep;3(9):569-73. doi: 10.1046/j.1365-2443.1998.00212.x. Genes Cells. 1998. PMID: 9813107 Review.

Shigetomi K, Ikenouchi J. Shigetomi K, et al. J Biochem. 2018 Apr 1;163(4):265-272. doi: 10.1093/jb/mvx077. J Biochem. 2018. PMID: 29186552 Review.

Cited by

Lu Q, Xie Y, Luo J, Gong Q, Li C. Lu Q, et al. Front Pharmacol. 2023 Jun 1;14:1168990. doi: 10.3389/fphar.2023.1168990. eCollection 2023. Front Pharmacol. 2023. PMID: 37324477 Free PMC article. Review.

Nie H, Zhang Y, Duan S, Zhang Y, Xu Y, Zhan J, Wen Y, Wu X. Nie H, et al. Life (Basel). 2022 Nov 4;12(11):1787. doi: 10.3390/life12111787. Life (Basel). 2022. PMID: 36362939 Free PMC article.

Bolla BS, Erdei L, Urbán E, Burián K, Kemény L, Szabó K. Bolla BS, et al. Sci Rep. 2020 Jul 30;10(1):12815. doi: 10.1038/s41598-020-69677-6. Sci Rep. 2020. PMID: 32733073 Free PMC article.

Gorzelanny C, Mess C, Schneider SW, Huck V, Brandner JM. Gorzelanny C, et al. Pharmaceutics. 2020 Jul 20;12(7):684. doi: 10.3390/pharmaceutics12070684. Pharmaceutics. 2020. PMID: 32698388 Free PMC article. Review.

Brown SJ, Elias MS, Bradley M. Brown SJ, et al. Acta Derm Venereol. 2020 Jun 9;100(12):adv00163. doi: 10.2340/00015555-3513. Acta Derm Venereol. 2020. PMID: 32412647 Free PMC article. Review.