Quantitative mapping of human hair greying and reversal in relation to life stress.

Ayelet M Rosenberg,Junting Ren,Desmond J Tobin,Rajesh Kumar Soni,Eugene V Mosharov,Purvi Patel,Shannon Rausser,Ralf Paus,Clay Lacefield,R Todd Ogden,Gabriel Sturm,Martin Picard

doi:10.7554/elife.67437

Ayelet M Rosenberg, Junting Ren + Show 10 more

Open Access

https://doi.org/10.7554/elife.67437

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Abstract

Hair greying is a hallmark of aging generally believed to be irreversible and linked to psychological stress. Here, we develop an approach to profile hair pigmentation patterns (HPPs) along individual human hair shafts, producing quantifiable physical timescales of rapid greying transitions. Using this method, we show white/grey hairs that naturally regain pigmentation across sex, ethnicities, ages, and body regions, thereby quantitatively defining the reversibility of greying in humans. Molecularly, grey hairs upregulate proteins related to energy metabolism, mitochondria, and antioxidant defenses. Combining HPP profiling and proteomics on single hairs, we also report hair greying and reversal that can occur in parallel with psychological stressors. To generalize these observations, we develop a computational simulation, which suggests a threshold-based mechanism for the temporary reversibility of greying. Overall, this new method to quantitatively map recent life history in HPPs provides an opportunity to longitudinally examine the influence of recent life exposures on human biology. This work was supported by the Wharton Fund and NIH grants GM119793, MH119336, and AG066828 (MP).

Highlights

Hair greying is a ubiquitous, visible, and early feature of human biological aging (O’Sullivan et al, 2021; Tobin, 2011)
We confirmed that compared to dark hairs still harboring their ‘young’ pigmentary state, the hair follicle pigmentary unit (HFPU) of ‘aged’ white HFs from either African American or Caucasian individuals are practically devoid of pigment (Figure 1D), which is consistent with the finding of previous studies (Cho et al, 2014)
Aiming for the simplest model that accounts for these known features of hair greying dynamics, we found a satisfactory model with three components (Figure 5B): (1) an ‘aging factor’ that progressively accumulates within each hair follicle, based on the fact that biological aging is more accurately modeled with the accumulation of damage, rather than a decline in stem cells or other reserves (Kinzina et al, 2019); (2) a biological threshold, beyond which hairs undergo depigmentation, characterizing the transition between the dark and white states in the same hair shafts (HSs); and (3) a ‘stress factor’ that acutely but reversibly increases the aging factor during a stressful event

Summary

Introduction

Hair greying is a ubiquitous, visible, and early feature of human biological aging (O’Sullivan et al, 2021; Tobin, 2011). Research in mice suggests stress may accelerate hair greying, but there is no definitive research on this in humans. This is because there are no research tools to precisely map stress and hair color over time. Combining HPP profiling and proteomics on single hairs, we report hair greying and reversal that can occur in parallel with psychological stressors. To generalize these observations, we develop a computational simulation, which suggests a threshold-based mechanism for the temporary reversibility of greying.

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