Single-cell transcriptomics reveals age-resistant maintenance of cell identities, stem cell compartments and differentiation trajectories in long-lived naked mole-rats skin

Savina, Aleksandra; Jaffredo, Thierry; Saldmann, Frédéric; Faulkes, Chris G.; Moguelet, Philippe; Leroy, Christine; Marmol, Delphine Del; Codogno, Patrice; L, Foucher; Zalc, Antoine; Viltard, Mélanie; Friedlander, Gérard; Aractingi, S.; Fontaine, R

doi:10.18632/aging.204054

Cited by 6 publications

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References 54 publications

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“…In agreement, the collection of key molecular modules participating in sebum production in aquatic or semi-aquatic mammals was shown to mirror such mosaic of skin morphologies: being fully absent in cetaceans but partially eroded in manatees and hippopotamuses (Lopes-Marques et al 2019a , b ; Themudo et al 2020 ; Springer et al 2021 ). Extreme skin modifications are not restricted to aquatic species and include the naked mole rat and pangolins (Menon et al 2019 ; Li et al 2020 ; Savina et al 2022 ). Species from the order Pholidota display a formidable keratin-scale armor probably serving as a key deterrent against predators and infections (Fig.…”

Section: Introductionmentioning

confidence: 99%

Decay of Skin-Specific Gene Modules in Pangolins

et al. 2023

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The mammalian skin exhibits a rich spectrum of evolutionary adaptations. The pilosebaceous unit, composed of the hair shaft, follicle, and the sebaceous gland, is the most striking synapomorphy. The evolutionary diversification of mammals across different ecological niches was paralleled by the appearance of an ample variety of skin modifications. Pangolins, order Pholidota, exhibit keratin-derived scales, one of the most iconic skin appendages. This formidable armor is intended to serve as a deterrent against predators. Surprisingly, while pangolins have hair on their abdomens, the occurrence of sebaceous and sweat glands is contentious. Here, we explore various molecular modules of skin physiology in four pangolin genomes, including that of sebum production. We show that genes driving wax monoester formation, Awat1/2, show patterns of inactivation in the stem pangolin branch, while the triacylglycerol synthesis gene Dgat2l6 seems independently eroded in the African and Asian clades. In contrast, Elovl3 implicated in the formation of specific neutral lipids required for skin barrier function is intact and expressed in the pangolin skin. An extended comparative analysis shows that genes involved in skin pathogen defense and structural integrity of keratinocyte layers also show inactivating mutations: associated with both ancestral and independent pseudogenization events. Finally, we deduce that the suggested absence of sweat glands is not paralleled by the inactivation of the ATP-binding cassette transporter Abcc11, as previously described in Cetacea. Our findings reveal the sophisticated and complex history of gene retention and loss as key mechanisms in the evolution of the highly modified mammalian skin phenotypes.

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Section: Introductionmentioning

confidence: 99%

Decay of Skin-Specific Gene Modules in Pangolins

et al. 2023

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“…In agreement, the collection of key molecular modules participating in sebum production in aquatic or semi-aquatic mammals was shown to mirror such mosaic of skin morphologies: being fully absent in cetaceans but only partially eroded in manatees and hippopotamuses (Lopes-Marques et al, 2019; Themudo et al, 2020; Springer et al 2021). Extreme skin modifications are not restricted to aquatic species and include the naked mole rat and pangolins (Menon et al 2019; Li et al 2020; Savina et al 2022). Species from the order Pholidota display a formidable keratin-scale armor probably serving as a key deterrent against predators and infections (Figure 1) (Meyer et al, 2013; Choo et al 2016; Li et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Convergent Decay of Skin-specific Gene Modules in Pangolins

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et al. 2022

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The Mammalia skin exhibits a rich spectrum of evolutionary adaptations. The pilosebaceous unit, composed of the hair shaft, follicle, and the sebaceous gland, is the most striking synapomorphy. The evolutionary diversification of mammals across different ecological niches was paralleled by the appearance of an ample variety of skin modifications. Pangolins, order Pholidota, exhibit keratin-derived scales, one of the most iconic skin appendages. This formidable armor is intended to serve as a key deterrent against predators. Surprisingly, while pangolins have hair on their abdomens, the occurrence of sebaceous and sweat glands is contentious. Here, we explore various molecular modules of skin physiology in four pangolin genomes, including that of sebum production. We show that genes driving wax monoester formation - Awat1/2, show patterns of inactivation in the stem pangolin branch; while the triacylglycerol synthesis gene Dgat2l6 seems independently eroded in the African and Asian clades. In contrast, Elovl3 implicated in the formation of specific neutral lipids required for skin barrier function, is intact and expressed in the skin. An extended comparative analysis shows that genes involved in skin pathogen defense and structural integrity of keratinocyte layers also show inactivating mutations: associated with both ancestral and independent pseudogenization events. Finally, we deduce that the suggested absence of sweat glands is not paralleled by the inactivation of the ATP-binding cassette transporter Abcc11, as previously described in Cetacea. Our findings reveal the sophisticated, convergent and complex history of gene retention and loss as key mechanisms in the evolution of the highly modified mammalian skin phenotypes

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