Abstract
Our laboratory discovered nestin-expressing hair follicle stem cells and demonstrated their pluripotency. We have shown that nestin-positive and K15-negative multipotent hair follicle stem cells are located above the hair follicle bulge, and we termed these cells hair follicle pluripotent stem (hfPS) cells. We have previously shown that hair follicle stem cells can regenerate peripheral nerve and spinal cord. In the present study, we describe the embryonic development of the hair follicle stem cell area (hfPSCA), which is located above the bulge and below the sebaceous glands in the adult mouse. At embryonic day 16.5 (E16.5) of nestindriven GFP (ND-GFP) transgenic mice, which express nestin in hfPS cells, the ND-GFP hair follicle stem cells are located in mesenchymal condensates. At postnatal day 0 (P0), the ND-GFP-expressing cells are migrating to the upper part of the hair follicle from the dermal papilla. At P3, keratin 15 (K15)-positive cells, derived from ND-GFP dermal papilla cells, are located in the outer-root sheath and basal layer of the epidermis. By P10, the ND-GFP have formed the K15-positive outer-root sheath as well as the ND-GFP hfPSA. These results suggest that ND-GFP hfPS cells in the dermal papilla form nestin-expressing hair follicle stem cells in the first hair cycle. These observations provide new insight into the origins of hfPS cells and the hfPSCA.
Similar content being viewed by others
References
Li L, Mignone J, Yang M, Matic M, Penman S, Enikolopov G, Hoffman RM (2003) Nestin expression in hair follicle sheath progenitor cells. Proc Natl Acad Sci U S A 100:9958–9961
Amoh Y, Li L, Katsuoka K, Penman S, Hoffman RM (2005) Multipotent nestin-positive, keratin-negative hair-follicle-bulge stem cells can form neurons. Proc Natl Acad Sci USA 102: 5530–5534
Amoh Y, Kanoh M, Niiyama S., Kawahara K, Sato Y, Katsuoka K, Hoffman RM (2009) Human and mouse hair follicles contain both multipotent and monopotent stem cells. Cell Cycle 8(1): 176–177
Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S, Hoffman RM (2005) Implanted hair follicle stem cells form Schwann cells which support repair of severed peripheral nerves. Proc Natl Acad Sci USA 102:17734–17738
Lendahl U, Zimmerman LB, McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585–595
Sawamoto K, Nakao N, Kobayashi K, Matsushita N, Takahashi H, Kakishita K, Yamamoto A, Yoshizaki T, Terashima T, Murakami F, Itakura T, Okano H (2001) Visualization, direct isolation, and transplantation of midbrain dopaminergic neurons. Proc Natl Acad Sci U S A 98:6423–6428
Amoh Y, Li L, Katsuoka K, Hoffman RM (2009) Multipotent nestin-expressing hair follicle stem cells. J Dermatol 36:1–9
Amoh Y, Kanoh M, Niiyama S, Hamada Y, Kawahara K, Sato Y, Hoffman RM, Katsuoka K (2009) Human hair follicle pluripotent stem (HFPS) cells promote regeneration of peripheral-nerve injury: an alternative to ES and iPS cells. J Cell Biochem 107:1016–1020
Amoh Y, Li L, Yang M, Moossa AR, Katsuoka K, Penman S, Hoffman RM (2004) Nascent blood vessels in the skin arise from nestin-expressing hair follicle cells. Proc Natl Acad Sci USA 101: 13291–13295
Dezawa M (2008) Systematic neuronal and muscle induction systems in bone marrow stromal cells: the potential for tissue reconstruction in neurodegenerative and muscle degenerative diseases. Med Mol Morphol 41:14–19
Hori Y (2009) Insulin-producing cells derived from stem/progenitor cells: therapeutic implications for diabetes mellitus. Med Mol Morphol 42:195–200
Amoh Y, Li L, Katsuoka K, Hoffman RM (2008) Multipotent hair follicle stem cells promote repair of spinal cord injury and recovery of walking function. Cell Cycle 7:1865–1869
Liu X, Driskell RR, Luo M, Abbott D, Filali M, Cheng N, Sigmund CD, Engelhardt JF (2004) Characterization of Lef-1 promoter segments that fascilitate inductive developmental expression in skin. J Invest Dermatol 123:264–274
Mignone JL, Kukekov V, Chiang A-S, Steindler D, Enikolovop G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311–324
Hoffman RM (2000) The hair follicle as a gene therapy target. Nat Biotechnol 18:20–21
Cotsarelis G, Sun TT, Lavker RM (1990) Label-retaining cells reside in the stem cell area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61:1329–1337
Mignone JL, Roig-Lopez JL, Fedstova N, Schones DE, Manganas LN, Maletic-Savatic M, Keyes WM, Mills AA, Gleiberman A, Zhang MQ, Enikolovop G (2007) Neural potential of a stem cell population in the hair follicle. Cell Cycle 6:2161–2170
Yu H, Fang D, Kumar SM, Li L, Nguyen TK, Acs G, Herlyn M, Xu X (2006) Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 168:1879–1888
Sieber-Blum M, Grim M, Hu Y-F, Szeder V (2004) Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231: 258–269
Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, Morikawa S, Okada Y, Mabuchi Y, Katoh H, Okada S, Fukuda K, Suda T, Matsuzaki Y, Toyama Y, Okano H (2008) Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2:392–403
Fernandes KJL, Toma JG, Miller FD (2008) Multipotent skinderived precursors: adult neural crest-related precursors with therapeutic potential. Philos Trans R Soc B 363:185–198
Biernaskie J, Paris M, Morozova O, Fagan BM, Marra M, Pevny L, Miller FD (2009) SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 4:610–623
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Amoh, Y., Li, L., Katsuoka, K. et al. Embryonic development of hair follicle pluripotent stem (hfPS) cells. Med Mol Morphol 43, 123–127 (2010). https://doi.org/10.1007/s00795-010-0498-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00795-010-0498-z