Hair follicle epidermal stem cells define a niche for tactile sensation
Chun-Chun Cheng,
Ko Tsutsui,
Toru Taguchi,
Noriko Sanzen,
Asako Nakagawa,
Kisa Kakiguchi,
Shigenobu Yonemura,
Chiharu Tanegashima,
Sean D Keeley,
Hiroshi Kiyonari,
Yasuhide Furuta,
Yasuko Tomono,
Fiona M Watt,
Hironobu Fujiwara
Affiliations
Chun-Chun Cheng
Laboratory for Tissue Microenvironment, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Ko Tsutsui
Laboratory for Tissue Microenvironment, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Toru Taguchi
Department of Neuroscience II, Research Institute of Environmental Medicine, Nagoya University, Nagoya, Japan; Department of Physical Therapy, Niigata University of Health and Welfare, Niigata, Japan
Noriko Sanzen
Laboratory for Tissue Microenvironment, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Asako Nakagawa
Laboratory for Tissue Microenvironment, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Kisa Kakiguchi
Laboratory for Ultrastructural Research, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Shigenobu Yonemura
Laboratory for Ultrastructural Research, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan; Department of Cell Biology, Tokushima University Graduate School of Medical Science, Tokushima, Japan
Chiharu Tanegashima
Laboratory for Phyloinformatics, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Sean D Keeley
Phyloinformatics Unit, RIKEN Center for Life Science Technologies, Kobe, Japan
Hiroshi Kiyonari
Laboratories for Animal Resource Development and Genetic Engineering, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Yasuhide Furuta
Laboratories for Animal Resource Development and Genetic Engineering, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Yasuko Tomono
Division of Molecular and Cell Biology, Shigei Medical Research Institute, Okayama, Japan
The heterogeneity and compartmentalization of stem cells is a common principle in many epithelia, and is known to function in epithelial maintenance, but its other physiological roles remain elusive. Here we show transcriptional and anatomical contributions of compartmentalized epidermal stem cells in tactile sensory unit formation in the mouse hair follicle. Epidermal stem cells in the follicle upper-bulge, where mechanosensory lanceolate complexes innervate, express a unique set of extracellular matrix (ECM) and neurogenesis-related genes. These epidermal stem cells deposit an ECM protein called EGFL6 into the collar matrix, a novel ECM that tightly ensheathes lanceolate complexes. EGFL6 is required for the proper patterning, touch responses, and αv integrin-enrichment of lanceolate complexes. By maintaining a quiescent original epidermal stem cell niche, the old bulge, epidermal stem cells provide anatomically stable follicle–lanceolate complex interfaces, irrespective of the stage of follicle regeneration cycle. Thus, compartmentalized epidermal stem cells provide a niche linking the hair follicle and the nervous system throughout the hair cycle.
