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A Genetic Basis of Variation in Eccrine Sweat Gland and Hair Follicle Density

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A Genetic Basis of Variation in Eccrine Sweat Gland and Hair Follicle Density A genetic basis of variation in eccrine sweat gland and hair follicle density Yana G. Kamberova,b,c,d,e, Elinor K. Karlssonc,e,1, Gerda L. Kamberovaf, Daniel E. Liebermand, Pardis C. Sabetic,e, Bruce A. Morganb,2, and Clifford J. Tabina,2 aDepartment of Genetics, Harvard Medical School, Boston, MA 02115; bDepartment of Dermatology, Harvard Medical School and Cutaneous Biology Research Center, Mass General Hospital, Charlestown, MA 02129; cThe Broad Institute of MIT and Harvard, Cambridge, MA 02142; dDepartment of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138; eCenter for Systems Biology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138; and fDepartment of Computer Science, Hofstra University, Hempstead, NY 11549 Contributed by Clifford J. Tabin, June 16, 2015 (sent for review March 7, 2015; reviewed by Cynthia Loomis and John C. Schimenti) Among the unique features of humans, one of the most salient is the Old World monkeys and apes, and which was subsequently ability to effectively cool the body during extreme prolonged activity elaborated in humans (3, 5). In contrast, eccrine glands in most through the evapotranspiration of water on the skin’s surface. The other mammals are restricted to the hairless friction pads, or evolution of this novel physiological ability required a dramatic in- footpads, of the fore and hindfeet where they serve a role in crease in the density and distribution of eccrine sweat glands relative traction rather than thermoregulation (5, 6). As a consequence, to other mammals and a concomitant reduction of body hair cover. studies to address the patterning relationship, if any, between Elucidation of the genetic underpinnings for these adaptive changes these two organ types have been limited by the lack of a tractable is confounded by a lack of knowledge about how eccrine gland fate model system in which eccrine glands and hair follicles are in- and density are specified during development. Moreover, although terspersed as in human skin. reciprocal changes in hair cover and eccrine gland density are re- Both hair follicles and eccrine glands are ectodermal append- quired for efficient thermoregulation, it is unclear if these changes ages that arise through a series of reciprocal interactions between are linked by a common genetic regulation. To identify pathways the embryonic ectoderm and underlying dermis (7). Work in controlling the relative patterning of eccrine glands and hair follicles, model systems, particularly the mouse, as well as the mapping of BIOLOGY we exploited natural variation in the density of these organs be- causal genetic mutations underlying clinical cases of ectodermal DEVELOPMENTAL tween different strains of mice. Quantitative trait locus mapping dysplasia in humans have implicated a number of common mo- identified a large region on mouse Chromosome 1 that controls both lecular pathways as critical in the formation of both eccrine hair and eccrine gland densities. Differential and allelic expression glands and hair follicles. These include the canonical Wnt, BMP, analysis of the genes within this interval coupled with subsequent Ectodysplasin, and Shh pathways (7–9). However, the molecular functional studies demonstrated that the level of En1 activity directs program that specifically leads to the formation of eccrine glands the relative numbers of eccrine glands and hair follicles. These find- as opposed to hair follicles and the distinct mechanisms that En1 ings implicate as a newly identified and reciprocal determinant govern eccrine gland patterning are poorly understood. of hair follicle and eccrine gland density and identify a pathway that Given the critical role that increased eccrine gland density could have contributed to the evolution of the unique features of has played in human physiology we investigated the genetic human skin. factors that control the density of these organs. Direct study of the genetic regulation of eccrine gland density in humans is eccrine sweat gland | hair follicle | ectodermal placode | engrailed 1 | ectodermal appendage Significance he maintenance of internal temperature homeostasis is critical Humans have the highest density of eccrine sweat glands of Tto the survival of all endotherms. In humans, cooling is mainly any mammal. Alongside hair follicles, eccrine glands are found achieved by the evaporation of water secreted by ubiquitously “ ” throughout human skin and are indispensible for thermoreg- distributed eccrine sweat glands from a furless skin surface (1). ulation. Despite their importance, little is known about the Human skin exhibits the highest reported density of eccrine sweat biological factors that control eccrine gland formation and glands of any mammal in combination with a diminution in the density. We investigated the genetic basis for the regulation of size of the vast majority of body hair. As a result, human skin is eccrine gland density in mice and find that eccrine gland and dramatically different in comparison with that of other primates hair follicle densities are inversely regulated by the transcrip- and facilitates efficient evaporative eccrine cooling. tion factor En1. This work uncovers a previously unidentified The increase in eccrine gland density and the reduction in biological factor that specifically promotes the development of body hair size are adaptations that almost certainly evolved in eccrine glands when these organs are interspersed with hair the hominin lineage. These traits are thought to have facilitated follicles, and has the potential to inform efforts to elucidate the long distance trekking in open habitats in the genus Austral- genetic basis for the evolution of increased eccrine gland opithecus, and were likely critical for the evolution of endurance density in humans. running capabilities in Homo (2, 3). In modern humans, this system of thermoregulation is still the main mechanism for dis- Author contributions: Y.G.K., D.E.L., P.C.S., B.A.M., and C.J.T. designed research; Y.G.K. performed research; Y.G.K., E.K.K., G.L.K., B.A.M., and C.J.T. analyzed data; and Y.G.K., sipating body heat, and thus dysfunction or loss through disease D.E.L., P.C.S., B.A.M., and C.J.T. wrote the paper. or injury leads to significant clinical morbidity (4). As a conse- Reviewers: C.L., NYU; and J.C.S., Cornell University. quence, elucidation of the molecular program governing the The authors declare no conflict of interest. development, patterning and evolution of these organs is of in- 1Present address: Program in Bioinformatics and Integrative Biology and Program in terest to the field of comprehensive skin regeneration. Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605. Hair follicles have a conserved evolutionary role in mamma- 2To whom correspondence may be addressed. Email: [email protected] or lian temperature regulation. However, ubiquitously distributed [email protected]. eccrine glands appear to be a relatively late innovation that first This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. appears in the catarrhines, the group of primates composed of 1073/pnas.1511680112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1511680112 PNAS Early Edition | 1of6 Downloaded by guest on September 28, 2021 challenging because invasive methods are required to accurately for all footpads scored). Footpads lack hair follicles in both strains score these organs in hairy skin (10). However, experimental (Fig. 1 A and C). evidence indicates that the early development of ectodermally derived appendages is conserved in vertebrates (7, 11). We A Complex Genetic Basis for Strain Differences in Ectodermal Appendage therefore turned to the laboratory mouse, a tractable genetic Density. To examine the genetic architecture underlying differences system. A rare exception among mammals, the mouse has both in eccrine gland and hair follicle number in the two strains, we hair and eccrine glands interspersed in a distinct domain of the generated F2 animals from an FVB/N by C57BL/6 cross. Analysis hindfoot where the density of the two appendage types can be of the trait distribution in the F2 population (n = 647) indicated a easily scored. Genetic mapping of the differences in patterns of polygenic basis for both phenotypes (Fig. 1 D and E). Comparison ectodermal appendages between mouse strains as well as func- of eccrine gland and hair follicle number in F2 individuals shows tional modulation of expression levels, implicate the transcription that, at the extremes, there is an inverse correlation between the factor En1 as a determinant of eccrine gland and hair follicle densities of the two appendage types (Fig. 1F). However, this in- densities in mice. These results reveal a hereto unappreciated verse correlation is not a simple reciprocal relationship, as statistical role for En1 in later patterning of the distal limb in mice and may analysis between hair follicle and eccrine gland number in F2 ani- provide clues as to the molecular pathways that were modified mals did not support a linear dependence between the two traits during human evolution to drive changes in eccrine gland density. [correlation coefficient is −0.5622, with 95% confidence interval (−0.6127 to −0.5070)]. However, analysis of the P value to test for Results a correlation between hair follicle and eccrine gland number, Strain-Specific Differences in Ectodermal Appendage Densities of Mice.
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