Dermal damage promoted by repeated low-level UV-A1 exposure despite tanning response in human skin

Abstract

Importance: Solar UV irradiation causes photoaging, characterized by fragmentation and reduced production of type I collagen fibrils that provide strength to skin. Exposure to UV-B irradiation (280-320 nm) causes these changes by inducing matrix metalloproteinase 1 and suppressing type I collagen synthesis. The role of UV-A irradiation (320-400 nm) in promoting similar molecular alterations is less clear yet important to consider because it is 10 to 100 times more abundant in natural sunlight than UV-B irradiation and penetrates deeper into the dermis than UV-B irradiation. Most (approximately 75%) of solar UV-A irradiation is composed of UV-A1 irradiation (340-400 nm), which is also the primary component of tanning beds.

Objective: To evaluate the effects of low levels of UV-A1 irradiation, as might be encountered in daily life, on expression of matrix metalloproteinase 1 and type I procollagen (the precursor of type I collagen).

Design, setting, and participants: In vivo biochemical analyses were conducted after UV-A1 irradiation of normal human skin at an academic referral center. Participants included 22 healthy individuals without skin disease.

Main outcomes and measures: Skin pigmentation was measured by a color meter (chromometer) under the L* variable (luminescence), which ranges from 0 (black) to 100 (white). Gene expression in skin samples was assessed by real-time polymerase chain reaction.

Results: Lightly pigmented human skin (L* >65) was exposed up to 4 times (1 exposure/d) to UV-A1 irradiation at a low dose (20 J/cm2), mimicking UV-A levels from strong sun exposure lasting approximately 2 hours. A single exposure to low-dose UV-A1 irradiation darkened skin slightly and did not alter matrix metalloproteinase 1 or type I procollagen gene expression. With repeated low-dose UV-A1 irradiation, skin darkened incrementally with each exposure. Despite this darkening, 2 or more exposures to low-dose UV-A1 irradiation significantly induced matrix metalloproteinase 1 gene expression, which increased progressively with successive exposures. Repeated UV-A1 exposures did not suppress type I procollagen expression.

Conclusions and relevance: A limited number of low-dose UV-A1 exposures, as commonly experienced in daily life, potentially promotes photoaging by affecting breakdown, rather than synthesis, of collagen. Progressive skin darkening in response to repeated low-dose UV-A1 exposures in lightly pigmented individuals does not prevent UV-A1-induced collagenolytic changes. Therefore, for optimal protection against skin damage, sunscreen formulations should filter all UV wavelengths, including UV-A1 irradiation.

Conflict of interest statement

Conflict of interest: The authors state no conflict of interest.

Figures

Figure 1. Exposure of lightly pigmented human skin to UVA1 irradiation causes skin darkening, induction of matrix metalloproteinases, and suppression of procollagens in a dose-dependent fashion

Skin pigmentation was measured using a color meter (chromameter) under the L* variable (luminescence), which ranges from 0 (black) to 100 (white). Lightly pigmented (L*>65) buttock skin of healthy human subjects (n=10) was exposed to the indicated doses of UVA1 irradiation. (a) Changes in skin pigmentation were measured 24 hours later (L* value, n=10). (b) Additionally, skin samples (4 mm) were obtained 24 hours following exposure, and real-time polymerase chain reaction was performed to assess gene expression of matrix metalloproteinase (MMP)-1, MMP-3, type I procollagen (COL-I), and type III procollagen (COL-III) (all n=10). The housekeeping gene acidic ribosomal phosphoprotein P0 (36B4) was used as an internal control. Data are presented as mean fold change + SEM. Asterisk (*) over bars, p<0.05 compared with no UVA1 irradiation. Asterisk (*) over bracket, p<0.05 when comparing response to different UVA1 doses.

Figure 2. Repeated daily exposure of lightly pigmented human skin to low-dose UVA1 irradiation causes incremental darkening and progressive induction of matrix metalloproteinases

Skin pigmentation was measured using a color meter (chromameter) under the L* variable (luminescence). Lightly pigmented (L*>65) buttock skin of healthy human subjects (n=12) was exposed to low-dose UVA1 irradiation (20 J/cm2) one, two, three, or four times at daily intervals. (a) Changes in skin pigmentation were measured 24 hours after each exposure (L* value, n=12). (b) Skin samples (4 mm) were also obtained 24 hours following each exposure, and real-time polymerase chain reaction was performed to assess gene expression of matrix metalloproteinase (MMP)-1, MMP-3, type I procollagen (COL-I), and type III procollagen (COL-III) (all n=12). The housekeeping gene acidic ribosomal phosphoprotein P0 (36B4) was used as an internal control. Data are presented as mean fold change + SEM. Asterisk (*) over bars, p<0.05 compared with no UVA1 irradiation. Asterisk (*) over bracket, p<0.05 when comparing response to different UVA1 exposures.