By protecting against cutaneous inflammation, epidermal pigmentation provided an additional advantage for ancestral humans

Tzu Kai Lin, Mao Qiang Man, Katrina Abuabara, Joan S. Wakefield, Hamm ming Sheu, Jui chen Tsai, Chih Hung Lee, Peter M. Elias

Research output: Contribution to journalArticle

Abstract

Pigmentation evolved in ancestral humans to protect against toxic, ultraviolet B irradiation, but the question remains: “what is being protected?” Because humans with dark pigmentation display a suite of superior epidermal functions in comparison with their more lightly pigmented counterparts, we hypothesized and provided evidence that dark pigmentation evolved in Africa to support cutaneous function. Because our prior clinical studies also showed that a restoration of a competent barrier dampens cutaneous inflammation, we hypothesized that resistance to inflammation could have provided pigmented hominins with yet another, important evolutionary benefit. We addressed this issue here in two closely related strains of hairless mice, endowed with either moderate (Skh2/J) or absent (Skh1) pigmentation. In these models, we showed that (a) pigmented mice display a markedly reduced propensity to develop inflammation after challenges with either a topical irritant or allergen in comparison with their nonpigmented counterparts; (b) visible and histologic evidence of inflammation was paralleled by reduced levels of pro-inflammatory cytokines (i.e., IL-1α and INFα); (c) because depigmentation of Skh2/J mouse skin enhanced both visible inflammation and pro-inflammatory cytokine levels after comparable pro-inflammatory challenges, the reduced propensity to develop inflammation was directly linked to the presence of pigmentation; and (d) furthermore, in accordance with our prior work showing that pigment production endows benefits by reducing the surface pH of skin, acidification of albino (Skh1) mouse skin also protected against inflammation, and equalized cytokine levels to those found in pigmented skin. In summary, pigmentation yields a reduced propensity to develop inflammation, consistent with our hypothesis that dark pigmentation evolved in ancestral humans to provide a suite of barrier-linked benefits that now include resistance to inflammation.

Original languageEnglish
Pages (from-to)1960-1970
Number of pages11
JournalEvolutionary Applications
Volume12
Issue number10
DOIs
Publication statusPublished - 2019 Dec 1

Fingerprint

Pigmentation
pigmentation
skin
inflammation
Inflammation
Skin
skin (animal)
cytokines
mice
Cytokines
acidification
pigment
irradiation
Hairless Mouse
Irritants
Poisons
Hominidae
interleukin-1
allergens
Interleukin-1

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Agricultural and Biological Sciences(all)

Cite this

Lin, Tzu Kai ; Man, Mao Qiang ; Abuabara, Katrina ; Wakefield, Joan S. ; Sheu, Hamm ming ; Tsai, Jui chen ; Lee, Chih Hung ; Elias, Peter M. / By protecting against cutaneous inflammation, epidermal pigmentation provided an additional advantage for ancestral humans. In: Evolutionary Applications. 2019 ; Vol. 12, No. 10. pp. 1960-1970.
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abstract = "Pigmentation evolved in ancestral humans to protect against toxic, ultraviolet B irradiation, but the question remains: “what is being protected?” Because humans with dark pigmentation display a suite of superior epidermal functions in comparison with their more lightly pigmented counterparts, we hypothesized and provided evidence that dark pigmentation evolved in Africa to support cutaneous function. Because our prior clinical studies also showed that a restoration of a competent barrier dampens cutaneous inflammation, we hypothesized that resistance to inflammation could have provided pigmented hominins with yet another, important evolutionary benefit. We addressed this issue here in two closely related strains of hairless mice, endowed with either moderate (Skh2/J) or absent (Skh1) pigmentation. In these models, we showed that (a) pigmented mice display a markedly reduced propensity to develop inflammation after challenges with either a topical irritant or allergen in comparison with their nonpigmented counterparts; (b) visible and histologic evidence of inflammation was paralleled by reduced levels of pro-inflammatory cytokines (i.e., IL-1α and INFα); (c) because depigmentation of Skh2/J mouse skin enhanced both visible inflammation and pro-inflammatory cytokine levels after comparable pro-inflammatory challenges, the reduced propensity to develop inflammation was directly linked to the presence of pigmentation; and (d) furthermore, in accordance with our prior work showing that pigment production endows benefits by reducing the surface pH of skin, acidification of albino (Skh1) mouse skin also protected against inflammation, and equalized cytokine levels to those found in pigmented skin. In summary, pigmentation yields a reduced propensity to develop inflammation, consistent with our hypothesis that dark pigmentation evolved in ancestral humans to provide a suite of barrier-linked benefits that now include resistance to inflammation.",
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By protecting against cutaneous inflammation, epidermal pigmentation provided an additional advantage for ancestral humans. / Lin, Tzu Kai; Man, Mao Qiang; Abuabara, Katrina; Wakefield, Joan S.; Sheu, Hamm ming; Tsai, Jui chen; Lee, Chih Hung; Elias, Peter M.

In: Evolutionary Applications, Vol. 12, No. 10, 01.12.2019, p. 1960-1970.

Research output: Contribution to journalArticle

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