Multi-layered environmental regulation on the homeostasis of stem cells: The saga of hair growth and alopecia

Journal of Dermatological Science

Volumn 66, Issue 1, 2012, Pages 3-11

  Chen, Chih Chiang ^a   Chuong, Cheng Ming ^b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Adipose cell; Alopecia; Bmp; Dkk; Hair; Macro environment; Niche; Regeneration; Sfrp; Stem cell

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH RECEPTOR; SEX HORMONE; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ADULT STEM CELL; AGING; ALOPECIA; CELL ACTIVATION; CELL REGENERATION; CIRCADIAN RHYTHM; HAIR FOLLICLE; HAIR GROWTH; HAIR STEM CELL; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; INTRADERMAL ADIPOSE TISSUE; MALE TYPE ALOPECIA; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEASONAL VARIATION; STEM CELL; STEM CELL MOBILIZATION; STEM CELL NICHE; TISSUE REGENERATION;

ALOPECIA; CELLULAR MICROENVIRONMENT; HAIR; HOMEOSTASIS; HUMANS; REGENERATION; STEM CELLS;

EID: 84862823864     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2012.02.007     Document Type: Review

References (68)

1. Schofield R. The relationship between the spleen colony-forming cell and the hamatopopietic stem cell. A hypothesis. Blood Cells 1978, 4:7-25.
2. Oh I.H., Kwon K.R. Concise review: multiple niches for hematopoietic stem cell regulations. Stem Cells 2010, 28(7):1243-1249.
3. Booth C., Potten C.S. Gut instincts: thoughts on intestinal epithelial stem cells. J Clin Invest 2000, 105:1493-1499.
4. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716.
5. Li L., Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol 2005, 21:605-631.
6. Yoshida S. Stem cells in mammalian spermatogenesis. Dev Growth Differ 2010, 52(3):311-317.
7. Collins C.A., Olsen I., Zammit P.S., Heslop L., Petrie A., Partridge T.A., et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005, 122(2):289-301.
8. Kuang S., Gillespie M.A., Rudnicki M.A. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2008, 2(1):22-31.
9. Chuong CM, Randall VA, Widelitz RB, Wu P, Jiang TX. Physiological regeneration of skin appendages. Physiology. (Minor revision), 2012.
10. Moore K.A., Lemischka I.R. Stem cells and their niches. Science 2006, 311(5769):1880-1885.
11. Hughes M.W., Wu P., Jiang T.-X., Lin S.-J., Dong C.-Y., Li A., et al. In search of the Golden Fleece: unraveling principles of morphogenesis by studying the integrative biology of skin appendages. Integr Biol 2011, 3:388-407.
12. Huelsken J., Vogel R., Erdmann B., Cotsarelis G., Birchmeier W. β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 2001, 105:533-545.
13. Reddy S., Andl T., Bagasra A., Lu M.M., Epstein D.J., Morrisey E.E., et al. Characterization of Wnt gene expression in developing and postnatal hair follicles and identification ofWnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech Dev 2001, 107:69-82.
14. Lowry W.E., Blanpain C., Nowak J.A., Guasch G., Lewis L., Fuchs E., et al. Defining the impact of b-catenin/Tcf transactivation on epithelial stem cells. Genes Dev 2005, 19:1596-1611.
15. Butcher E.O. Hair growth on skin transplants in the immature albino rat. Anat Rec 1936, 64:161-171.
16. Plikus M.V., Chuong C.M. Complex hair cycle domain patterns and regenerative hair waves in living rodents. J Invest Dermatol 2008, 128:1071-1080.
17. Plikus M.V., Mayer J.A., de la Cruz D., Baker R.E., Maini P.K., Maxson R., et al. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 2008, 451(7176):340-344.
18. Plikus M.V., Widelitz R.B., Maxson R., Chuong C.M. Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. Int J Dev Biol 2009, 53(5-6):857-868.
19. Plikus M.V., Baker R.E., Chen C.C., Fare C., de la Cruz D., Andl T., et al. Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 2011, 332(6029):586-589.
20. Festa E., Fretz J., Berry R., Schmidt B., Rodeheffer M., Horowitz M., et al. Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 2011, 146(5):761-771.
21. Jahoda C.A., Christiano A.M. Niche crosstalk: intercellular signals at the hair follicle. Cell 2011, 146(5):678-681.
22. Nishikawa M., Ozawa K., Tojo A., Yoshikubo T., Okano A., Tani K., et al. Changes in hematopoiesis-supporting ability of C3H10T1/2 mouse embryo fibroblasts during differentiation. Blood 1993, 81:1184-1192.
23. Corre J., Barreau C., Cousin B., Chavoin J.P., Caton D., Fournial G., et al. Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors. J Cell Physiol 2006, 208:282-288.
24. Belaid-Choucair Z., Lepelletier Y., Poncin G., Thiry A., Humblet C., Maachi M., et al. Human bone marrow adipocytes block granulopoiesis through neuropilin-1-induced granulocyte colony-stimulating factor inhibition. Stem Cells 2008, 26:1556-1564.
25. Miharada K., Hiroyama T., Sudo K., Danjo I., Nagasawa T., Nakamura Y. Lipocalin 2-mediated growth suppression is evident in human erythroid and monocyte/macrophage lineage cells. J Cell Physiol 2008, 215:526-537.
26. Yan Q.W., Yang Q., Mody N., Graham T.E., Hsu C.H., Xu Z., et al. The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 2007, 56:2533-2540.
27. Yokota T., Oritani K., Takahashi I., Ishikawa J., Matsuyama A., Ouchi N., et al. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 2000, 96:1723-1732.
28. Zhang Y., Harada A., Bluethmann H., Wang J.B., Nakao S., Mukaida N., et al. Tumor necrosis factor (TNF) is a physiologic regulator of hematopoietic progenitor cells: increase of early hematopoietic progenitor cells in TNF receptor p55-deficient mice in vivo and potent inhibition of progenitor cell proliferation by TNF alpha in vitro. Blood 1995, 86:2930-2937.
29. Hotamisligil G.S., Shargill N.S., Spiegelman B.M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993, 259:87-91.
30. Naveiras O., Nardi V., Wenzel P.L., Hauschka P.V., Fahey F., Daley G.Q. Bone marrow adipocytes as negative regulators of the hematopoietic microenvironment. Nature 2009, 460(7252):259-263.
31. Thornton M.J., Taylor A.H., Mulligan K., Al-Azzawi F., Lyon C.C., O'Driscoll J., et al. The distribution of estrogen receptor beta is distinct to that of estrogen receptor alpha and the androgen receptor in human skin and the pilosebaceous unit. J Investig Dermatol Symp Proc 2003, 8:100-103.
32. Thornton M.J., Nelson L.D., Taylor A.H., Birch M.P., Laing I., Messenger A.G. The modulation of aromatase and estrogen receptor alpha in cultured human dermal papilla cells by dexamethasone: a novel mechanism for selective action of estrogen via estrogen receptor beta?. J Invest Dermatol 2006, 126:2010-2018.
33. Chang C.Y., Hsuuw Y.D., Huang F.J., Shyr C.R., Chang S.Y., Huang C.K., et al. Androgenic and antiandrogenic effects and expression of androgen receptor in mouse embryonic stem cells. Fertil Steril 2006, 85(Suppl. 1):1195-1203.
34. Han H.J., Heo J.S., Lee Y.J. Estradiol-17beta stimulates proliferation of mouse embryonic stem cells: involvement of MAPKs and CDKs as well as protooncogenes. Am J Physiol Cell Physiol 2006, 290(4):C1067-C1075.
35. Hong S.H., Nah H.Y., Lee Y.J., Lee J.W., Park J.H., Kim S.J., et al. Expression of estrogen receptor-alpha and -beta, glucocorticoid receptor, and progesterone receptor genes in human embryonic stem cells and embryoid bodies. Mol Cells 2004, 18(3):320-325.
36. Ray R., Novotny N.M., Crisostomo P.R., Lahm T., Abarbanell A., Meldrum D.R. Sex steroids and stem cell function. Mol Med 2008, 14(7-8):493-501.
37. Di Gregorio G.B., Yamamoto M., Ali A.A., Abe E., Roberson P., Manolagas S.C., et al. Attenuation of the self-renewal of transit-amplifying osteoblast progenitors in the murine bone marrow by 17 beta-estradiol. J Clin Invest 2001, 107(7):803-812.
38. Strehlow K., Werner N., Berweiler J., Link A., Dirnagl U., Priller J., et al. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation 2003, 107(24):3059-3065.
39. Asselin-Labat M.L., Vaillant F., Sheridan J.M., Pal B., Wu D., Simpson E.R., et al. Control of mammary stem cell function by steroid hormone signaling. Nature 2010, 465(7299):798-802.
40. Randall V.A. Hormonal regulation of hair follicles exhibits a biological paradox. Semin Cell Dev Biol 2007, 18(2):274-285.
41. Randall V.A., Thornton M.J., Messenger A.G. Cultured dermal papilla cells from androgen-dependent human hair follicles (e.g. beard) contain more androgen receptors than those from non-balding areas of scalp. J Endocrinol 1992, 3:141-147.
42. Hamada K., Thornton M.J., Laing I., Messenger A.G., Randall V.A. The metabolism of testosterone by dermal papilla cells cultured from human pubic and axillary hair follicles concurs with hair growth in 5 alpha-reductase deficiency. J Invest Dermatol 1996, 106(5):1017-1022.
43. Hibberts N.A., Howell A.E., Randall V.A. Dermal papilla cells from human balding scalp hair follicles contain higher levels of androgen receptors than those from non-balding scalp. J Endocrinol 1998, 156:59-65.
44. Ando Y., Yamaguchi Y., Hamada K., Yoshikawa K., Itami S. Expression of mRNAfor androgen receptor, 5α-reductase and 17β-hydroxysteroid dehydrogenase in human dermal papilla cells. Br J Dermatol 1999, 141:840-845.
45. Garza L.A., Yang C.C., Zhao T., Blatt H.B., Lee M., He H., et al. Bald scalp in men with androgenetic alopecia retains hair follicle stem cells but lacks CD200-rich and CD34-positive hair follicle progenitor cells. J Clin Invest 2011, 121(2):613-622.
46. Calado R.T., Yewdell W.T., Wilkerson K.L., Regal J.A., Kajigaya S., Stratakis C.A., et al. Sex hormones, acting on the TERT gene, increase telomerase activity in human primary hematopoietic cells. Blood 2009, 114(11):2236-2243.
47. Koelling S., Miosge N. Sex differences of chondrogenic progenitor cells in late stages of osteoarthritis. Arthritis Rheum 2010, 62(4):1077-1087.
48. Sayama K., Kajiya K., Sugawara K., Sato S., Hirakawa S., Shirakata Y., et al. Inflammatory mediator TAK1 regulates hair follicle morphogenesis and anagen induction shown by using keratinocyte-specific TAK1-deficient mice. PLoS One 2010, 5(6):e11275.
49. Osaka N., Takahashi T., Murakami S., Matsuzawa A., Noguchi T., Fujiwara T., et al. ASK1-dependent recruitment and activation of macrophages induce hair growth in skin wounds. J Cell Biol 2007, 176(7):903-909.
50. Heo S.C., Jeon E.S., Lee I.H., Kim H.S., Kim M.B., Kim J.H. Tumor necrosis factor-α-activated human adipose tissue-derived mesenchymal stem cells accelerate cutaneous wound healing through paracrine mechanisms. J Invest Dermatol 2011, 131(7):1559-1567.
51. Duheron V., Hess E., Duval M., Decossas M., Castaneda B., Klöpper J.E., et al. Receptor activator of NF-kappaB (RANK) stimulates the proliferation of epithelial cells of the epidermo-pilosebaceous unit. Proc Natl Acad Sci USA 2011, 108(13):5342-5347.
52. Kollet O., Dar A., Shivtiel S., Kalinkovich A., Lapid K., Sztainberg Y., et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006, 12(June (6)):657-664.
53. Brownell I., Guevara E., Bai C.B., Loomis C.A., Joyner A.L. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 2011, 8(5):552-565.
54. Katayama Y., Battista M., Kao W.M., Hidalgo A., Peired A.J., Thomas S.A., et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006, 124(2):407-421.
55. Spiegel A., Kalinkovich A., Shivtiel S., Kollet O., Lapidot T. Stem cell regulation via dynamic interactions of the nervous and immune systems with the microenvironment. Cell Stem Cell 2008, 3(5):484-492.
56. Mayack S.R., Shadrach J.L., Kim F.S., Wagers A.J. Systemic signals regulate ageing and rejuvenation of blood stem cell niches. Nature 2010, 463(7280):495-500.
57. Conboy I.M., Conboy M.J., Wagers A.J., Girma E.R., Weissman I.L., Rando T.A. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433(7027):760-764.
58. Gopinath S.D., Rando T.A. Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell 2008, 7(4):590-598.
59. Méndez-Ferrer S., Chow A., Merad M., Frenette P.S. Circadian rhythms influence hematopoietic stem cells. Curr Opin Hematol 2009, 16(4):235-242.
60. Méndez-Ferrer S., Lucas D., Battista M., Frenette P.S. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008, 452(7186):442-447.
61. Kawai M., Green C.B., Lecka-Czernik B., Douris N., Gilbert M.R., Kojima S., et al. A circadian-regulated gene, nocturnin, promotes adipogenesis by stimulating PPAR-γ nuclear translocation. Proc Natl Acad Sci USA 2010, 107(23):10508-10513.
62. Lin K.K., Kumar V., Geyfman M., Chudova D., Ihler A.T., Smyth P., et al. Circadian clock genes contribute to the regulation of hair follicle cycling. PLoS Genet 2009, 5(7):e1000573.
63. Janich P., Pascual G., Merlos-Suárez A., Batlle E., Ripperger J., Albrecht U., et al. The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 2011, 480(7376):209-214.
64. Dicks P., Russel A.J., Lincoln G.A. The role of prolactin in the reactivation of hair follicles in relation to moulting in cashmere goats. J Endocrinol 1994, 143(3):441-448.
65. Lincoln G.A., Baker B.I. Seasonal and photoperiod-induced changes in the secretion of alpha-melanocyte-stimulating hormone in Soay sheep: temporal relationships with changes in beta-endorphin, prolactin, follicle-stimulating hormone, activity of the gonads and growth of wool and horns. J Endocrinol 1995, 144(3):471-481.
66. Randall V.A., Ebling F.J. Seasonal changes in human hair growth. Br J Dermatol 1991, 124(2):146-151.
67. Kunz M., Seifert B., Trüeb R.M. Seasonality of hair shedding in healthy women complaining of hair loss. Dermatology 2009, 219(2):105-110.
68. Lucas D., Battista M., Shi P.A., Isola L., Frenette P.S. Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 2008, 3(4):364-366.