A role for keratins in supporting mitochondrial organization and function in skin keratinocytes

Mitochondria fulfill essential roles in ATP production, metabolic regulation, calcium signaling, generation of reactive oxygen species (ROS), and additional determinants of cellular health. Recent studies have highlighted a role for mitochondria during cell differentiation, including in skin epiderm...

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Published inMolecular biology of the cell Vol. 31; no. 11; pp. 1103 - 1111
Main Authors Steen, Kaylee, Chen, Desu, Wang, Fengrong, Majumdar, Ritankar, Chen, Song, Kumar, Surinder, Lombard, David B, Weigert, Roberto, Zieman, Abigail G, Parent, Carole A, Coulombe, Pierre A
Format Journal Article
LanguageEnglish
Published United States The American Society for Cell Biology 15.05.2020
Subjects
Animals
Brief Reports
Cytoskeletal Proteins
Epidermis
Female
Keratin-16 - genetics
Keratin-16 - metabolism
Keratin-6 - genetics
Keratin-6 - metabolism
Keratinocytes - metabolism
Keratinocytes - physiology
Keratins - metabolism
Keratins - physiology
Keratoderma, Palmoplantar
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Mitochondria - metabolism
Mitochondria - physiology
Mutation
Pachyonychia Congenita
Skin - metabolism
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Abstract Mitochondria fulfill essential roles in ATP production, metabolic regulation, calcium signaling, generation of reactive oxygen species (ROS), and additional determinants of cellular health. Recent studies have highlighted a role for mitochondria during cell differentiation, including in skin epidermis. The observation of oxidative stress in keratinocytes from null mouse skin, a model for pachyonychia congenita (PC)-associated palmoplantar keratoderma, prompted us to examine the role of Keratin (K) 16 protein and its partner K6 in regulating the structure and function of mitochondria. Electron microscopy revealed major anomalies in mitochondrial ultrastructure in late stage, E18.5, null embryonic mouse skin. Follow-up studies utilizing biochemical, metabolic, and live imaging readouts showed that, relative to controls, skin keratinocytes null for or exhibit elevated ROS, reduced mitochondrial respiration, intracellular distribution differences, and altered movement of mitochondria within the cell. These findings highlight a novel role for K6 and K16 in regulating mitochondrial morphology, dynamics, and function and shed new light on the causes of oxidative stress observed in PC and related keratin-based skin disorders.
AbstractList We provide evidence that keratins (K) 6 and 16 modulate the organization, movement, and function of mitochondria in skin keratinocytes. Loss of either K6 or K16 protein results in reduced mitochondrial respiration and elevated reactive oxygen species. This newly defined role may be relevant to diseases caused by mutations in K6 or K16. Mitochondria fulfill essential roles in ATP production, metabolic regulation, calcium signaling, generation of reactive oxygen species (ROS), and additional determinants of cellular health. Recent studies have highlighted a role for mitochondria during cell differentiation, including in skin epidermis. The observation of oxidative stress in keratinocytes from Krt16 null mouse skin, a model for pachyonychia congenita (PC)–associated palmoplantar keratoderma, prompted us to examine the role of Keratin (K) 16 protein and its partner K6 in regulating the structure and function of mitochondria. Electron microscopy revealed major anomalies in mitochondrial ultrastructure in late stage, E18.5, Krt6a/Krt6b null embryonic mouse skin. Follow-up studies utilizing biochemical, metabolic, and live imaging readouts showed that, relative to controls, skin keratinocytes null for Krt6a/Krt6b or Krt16 exhibit elevated ROS, reduced mitochondrial respiration, intracellular distribution differences, and altered movement of mitochondria within the cell. These findings highlight a novel role for K6 and K16 in regulating mitochondrial morphology, dynamics, and function and shed new light on the causes of oxidative stress observed in PC and related keratin-based skin disorders.
Mitochondria fulfill essential roles in ATP production, metabolic regulation, calcium signaling, generation of reactive oxygen species (ROS), and additional determinants of cellular health. Recent studies have highlighted a role for mitochondria during cell differentiation, including in skin epidermis. The observation of oxidative stress in keratinocytes from Krt16 null mouse skin, a model for pachyonychia congenita (PC)–associated palmoplantar keratoderma, prompted us to examine the role of Keratin (K) 16 protein and its partner K6 in regulating the structure and function of mitochondria. Electron microscopy revealed major anomalies in mitochondrial ultrastructure in late stage, E18.5, Krt6a/Krt6b null embryonic mouse skin. Follow-up studies utilizing biochemical, metabolic, and live imaging readouts showed that, relative to controls, skin keratinocytes null for Krt6a/Krt6b or Krt16 exhibit elevated ROS, reduced mitochondrial respiration, intracellular distribution differences, and altered movement of mitochondria within the cell. These findings highlight a novel role for K6 and K16 in regulating mitochondrial morphology, dynamics, and function and shed new light on the causes of oxidative stress observed in PC and related keratin-based skin disorders.
Mitochondria fulfill essential roles in ATP production, metabolic regulation, calcium signaling, generation of reactive oxygen species (ROS), and additional determinants of cellular health. Recent studies have highlighted a role for mitochondria during cell differentiation, including in skin epidermis. The observation of oxidative stress in keratinocytes from null mouse skin, a model for pachyonychia congenita (PC)-associated palmoplantar keratoderma, prompted us to examine the role of Keratin (K) 16 protein and its partner K6 in regulating the structure and function of mitochondria. Electron microscopy revealed major anomalies in mitochondrial ultrastructure in late stage, E18.5, null embryonic mouse skin. Follow-up studies utilizing biochemical, metabolic, and live imaging readouts showed that, relative to controls, skin keratinocytes null for or exhibit elevated ROS, reduced mitochondrial respiration, intracellular distribution differences, and altered movement of mitochondria within the cell. These findings highlight a novel role for K6 and K16 in regulating mitochondrial morphology, dynamics, and function and shed new light on the causes of oxidative stress observed in PC and related keratin-based skin disorders.
Author Parent, Carole A
Lombard, David B
Weigert, Roberto
Zieman, Abigail G
Majumdar, Ritankar
Kumar, Surinder
Steen, Kaylee
Chen, Desu
Wang, Fengrong
Coulombe, Pierre A
Chen, Song
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Department of Molecular, Cellular and Developmental Biology, School of Medicine, Yale University, New Haven, CT 06511.
Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109
Present addresses: †Office of Research, University of Michigan Medical School, Ann Arbor, MI 48109
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Snippet Mitochondria fulfill essential roles in ATP production, metabolic regulation, calcium signaling, generation of reactive oxygen species (ROS), and additional...
We provide evidence that keratins (K) 6 and 16 modulate the organization, movement, and function of mitochondria in skin keratinocytes. Loss of either K6 or...
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SubjectTerms Animals
Brief Reports
Cytoskeletal Proteins
Epidermis
Female
Keratin-16 - genetics
Keratin-16 - metabolism
Keratin-6 - genetics
Keratin-6 - metabolism
Keratinocytes - metabolism
Keratinocytes - physiology
Keratins - metabolism
Keratins - physiology
Keratoderma, Palmoplantar
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Mitochondria - metabolism
Mitochondria - physiology
Mutation
Pachyonychia Congenita
Skin - metabolism
Title A role for keratins in supporting mitochondrial organization and function in skin keratinocytes
URI https://www.ncbi.nlm.nih.gov/pubmed/32213122
https://search.proquest.com/docview/2384199294
https://pubmed.ncbi.nlm.nih.gov/PMC7353162
Volume 31
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