Immune privilege and alopecia areata

References

• Billingham RE, Boswell T. Studies on the problem of corneal homografts. Proc. R. Soc. Lond. B Biol. Sci.141, 392–406 (1953).
   PubMed Web of Science ®Google Scholar
• Head JR, Billingham RE. Immunologically privileged sites in transplantation immunology and oncology. Perspect. Biol. Med.29, 115–131 (1985).
   PubMed Web of Science ®Google Scholar
• Mellor AL, Munn DH. Immunology at the maternal-fetal interface: lessons for T cell tolerance and suppression. Ann. Rev. Immunol.18, 367–391 (2000).
   PubMed Web of Science ®Google Scholar
• Erlebacher A. Why isn’t the fetus rejected? Curr. Opin. Immunol.13, 590–593 (2001).
   PubMed Web of Science ®Google Scholar
• Niederkorn JY. Immune privilege in the anterior chamber of the eye. Crit. Rev. Immunol.22, 13–46 (2002).
   PubMed Web of Science ®Google Scholar
• Paus R, Nickoloff BJ, Ito T. A ‘hairy’ privilege. Trends Immunol.26, 32–40 (2005).
   PubMed Web of Science ®Google Scholar
• Ito T, Ito N, Saathoff M et al. Immunology of the human nail apparatus: the nail matrix is a site of relative immune privilege. J. Invest. Dermatol.125, 1139–1148 (2005).
   PubMed Web of Science ®Google Scholar
• Streilein JW. Immune privilege as the result of local tissue barriers and immunosuppressive microenvironments. Curr. Opin. Immunol.5, 428–432 (1993).
   PubMed Web of Science ®Google Scholar
• Brent L. A History of Transplantation Immunology. Academic Press, CA, USA (1997).
   Google Scholar
• Janeway CA, Travers P, Walport M, Shlomchik MJ. Autoimmunity and transplantation. In: Immunobiology. Janeway CA (Ed.). Garland Publishers, NY, USA 557–612 (2001).
   Google Scholar
• Filippini A, Riccioli A, Padula F et al. Control and impairment of immune privilege in the testis and in semen. Hum. Reprod. Update7, 444–449 (2001).
   PubMed Web of Science ®Google Scholar
• Lobo-Yeo A, Senaldi G, Portmann B et al. Class I and class II major histocompatibility complex antigen expression on hepatocytes: a study in children with liver disease. Hepatology12, 224–232 (1990).
   PubMed Web of Science ®Google Scholar
• Franco A, Barnaba V, Natali P et al. Expression of class I and class II major histocompatibility complex antigens on human hepatocytes. Hepatology8, 449–454 (1988).
   PubMed Web of Science ®Google Scholar
• Munn DH, Zhou M, Attwood JT et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science281, 1191–1193 (1998).
   PubMed Web of Science ®Google Scholar
• Fallarino F, Grohmann U, Hwang KW et al. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol.4, 1206–1212 (2003).
   PubMed Web of Science ®Google Scholar
• Mellor AL, Chandler P, Baban B et al. Specific subsets of murine dendritic cells acquire potent T-cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase. Int. Immunol.16, 1391–1401 (2004).
   PubMed Web of Science ®Google Scholar
• Hobbs NK, Bondareva AA, Barnett S et al. Removing the vertebrate-specific TBP N terminus disrupts placental b2m-dependent interactions with the maternal immune system. Cell110, 43–54 (2002).
   PubMedGoogle Scholar
• Yamashita K, Ollinger R, McDaid J et al. Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J.20, 776–778 (2006).
   PubMedGoogle Scholar
• McDaid J, Yamashita K, Chora A et al. Heme oxygenase-1 modulates the allo-immune response by promoting activation-induced cell death of T cells. FASEB J.19, 458–460 (2005).
   PubMedGoogle Scholar
• Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol.24, 449–455 (2003).
   PubMed Web of Science ®Google Scholar
• Soares MP, Lin Y, Anrather J et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat. Med.4, 1073–1077 (1998).
   PubMed Web of Science ®Google Scholar
• Sato K, Balla J, Otterbein L et al. Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J. Immunol.166, 4185–4194 (2001).
   PubMedGoogle Scholar
• Yamashita K, McDaid J, Ollinger R et al. Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J.18, 765–767 (2004).
   PubMedGoogle Scholar
• Paul WE. Fundamental Immunology (Fifth Edition). Lippincott Williams & Wilkins, PA, USA (1999).
   Google Scholar
• Billingham RE. Transplantation immunity evoked by skin allografts and expressed in intact skin. In: Immunology of the Skin. Montagna W, Billingham RE (Eds). Appleton-Century-Crofts, NY, USA 183–198 (1971).
   Google Scholar
• Billingham RE, Silvers WK. A biologist’s reflections on dermatology. J. Invest. Dermatol.57, 227–240 (1971).
   PubMedGoogle Scholar
• Bröcker EB, Echternacht-Happle K, Hamm H, Happle R. Abnormal expression of class I and class II major histocompatibility antigen in alopecia areata. J. Invest. Dermatol.88, 564–568 (1987).
   PubMed Web of Science ®Google Scholar
• Westgate GE, Craggs RI, Gibson WT. Immune privilege in hair growth. J. Invest. Dermatol.97, 417–420 (1991).
   PubMed Web of Science ®Google Scholar
• Paus R, Eichmüller S, Hofmann U et al. Expression of classical and non-classical MHC class I antigens in murine hair follicles. Br. J. Dermatol.131, 177–183 (1994).
   PubMed Web of Science ®Google Scholar
• Christoph T, Müller-Röver S, Audring H et al. The human hair follicle immune system: cellular composition and immune privilege. Br. J. Dermatol.142, 862–873 (2000).
   PubMed Web of Science ®Google Scholar
• Welker P, Foitzik K, Bulfone-Paus S et al. Hair cycle-dependent changes in the gene expression and protein content of transforming factor-β1 and β3 in murine skin. Arch. Dermatol. Res.289, 554–557 (1997).
   PubMed Web of Science ®Google Scholar
• Foitzik K, Lindner G, Mueller-Roever S et al. Control of murine hair follicle regression (catagen) by TGF-β1 in vivo.FASEB J.14, 752–760 (2000).
   PubMed Web of Science ®Google Scholar
• Slominski A, Wortsman J, Mazurkiewicz JE et al. Detection of proopiomelanocortin-derived antigens in normal and pathologic human skin. J. Lab. Clin. Med.122, 658–666 (1993).
   PubMedGoogle Scholar
• Slominski A, Wortsman J, Luger T et al. Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. Physiol. Rev.80, 979–1020 (2000).
   PubMed Web of Science ®Google Scholar
• Paus R, Botchkarev VA, Botchkareva NV et al. The skin POMC system (SPS): leads and lessons from the hair follicle. Ann. NY Acad. Sci.885, 350–363 (1999).
   PubMedGoogle Scholar
• Botchkarev VA, Botchkareva NV, Slominski A et al. Developmentally regulated expression of α-MSH and MC-1 receptor in C57BL/6 mouse skin suggests functions beyond pigmentation. Ann. NY Acad. Sci.885, 433–439 (1999).
   PubMedGoogle Scholar
• Paus R, Hofmann U, Eichmüller S, Czarnetzki BM. Distribution and changing density of γ-δ T cells in murine skin during the induced hair cycle. Br. J. Dermatol.130, 281–289 (1994).
   PubMedGoogle Scholar
• Stenn KS, Paus R. Control of hair follicle cycling. Physiol. Rev.81, 449–494 (2001).
   PubMed Web of Science ®Google Scholar
• Billingham RE. The immunobiology of tissue transplantation. Int. Dent. J.21, 478–487 (1971).
   PubMedGoogle Scholar
• Reynolds AJ, Lawrence C, Cserhalmi-Friedman PB, Christiano AM, Jahoda CA. Trans-gender induction of hair follicles. Nature402(6757), 33–34 (1999).
   PubMed Web of Science ®Google Scholar
• Messenger AG. The control of hair growth and pigmentation. In: Disorders of Hair Growth (2nd Edition). Olsen EA (Ed.). McGraw-Hill, NY, USA 49–74 (2003).
   Google Scholar
• Harries MJ, Meyer KC, Paus R. Hair loss as a result of cutaneous autoimmunity: frontiers in the immunopathogenesis of primary cicatricial alopecia. Autoimmun. Rev.8, 478–483 (2009).
   PubMedGoogle Scholar
• Cotsarelis G. Epithelial stem cells: a folliculocentric view. J. Invest. Dermatol.126, 1459–1468 (2006).
   PubMed Web of Science ®Google Scholar
• Morris RJ, Liu Y, Marles L et al. Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol.22, 411–417 (2004).
   PubMed Web of Science ®Google Scholar
• Niederkorn JY. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat. Immunol.7, 354–359 (2006).
   PubMed Web of Science ®Google Scholar
• Siglienti I, Chan A, Kleinschnitz C et al. Downregulation of transforming growth factor-beta2 facilitates inflammation in the central nervous system by reciprocal astrocyte/microglia interactions. J. Neuropathol. Exp. Neurol.66, 47–56 (2007).
   PubMedGoogle Scholar
• Ohyama M, Terunuma A, Tock CL et al. Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J. Clin. Invest.116, 249–260 (2006).
   PubMed Web of Science ®Google Scholar
• Rosenblum MD, Olasz EB, Yancey KB et al. Expression of CD200 on epithelial cells of the murine hair follicle: a role in tissue-specific immune tolerance? J. Invest. Dermatol.123, 880–887 (2004).
   PubMed Web of Science ®Google Scholar
• Apte RS, Sinha D, Mayhew E et al. Cutting edge: role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege. J. Immunol.160, 5693–5696 (1998).
   PubMed Web of Science ®Google Scholar
• Meyer KC, Klatte JE, Dinh HV et al. Evidence that the bulge region is a site of relative immune privilege in human hair follicles. Br. J. Dermatol.159, 1077–1085 (2008).
   PubMed Web of Science ®Google Scholar
• Hainz U, Jürgens B, Heitger A. The role of indoleamine 2,3-dioxygenase in transplantation. Transpl. Int.20, 118–127 (2007).
   PubMed Web of Science ®Google Scholar
• Dawber R, Fenton DA. Infections and infestations. In: Disease of the Hair and Scalp (3rd Edition). Dawber R. (Ed.). Blackwell Science, Oxford, UK 418–460 (1997).
   Google Scholar
• Hermes B, Paus R. [Scar forming alopecia. Comments in classification, differenciatial diagnosis and pathobiology.] Hautarzt49, 462–472 (1998).
   PubMedGoogle Scholar
• Cotsarelis G, Millar SE. Towards a molecular understanding of hair loss and its treatment. Trends Mol. Med.7, 293–301 (2001).
   PubMed Web of Science ®Google Scholar
• Paus R, Christoph T, Müller-Rover S. Immunology of the hair follicle: a short journey into terra incognita. J. Invest. Dermatol. Symp. Proc.4, 226–234 (1999).
   PubMedGoogle Scholar
• Paus R, Slominski A, Czarnetzki BM. Is alopecia areata an autoimmune-response against melanogenesis-related proteins, Exposed by abnormal MHC class I expression in the anagen hair bulb. Yale J. Biol. Med.66, 541–554 (1994).
   Google Scholar
• Rezai-Zadeh K, Gate D, Town T. CNS infiltration of peripheral immune cells: D-day for neurodegenerative disease? J. Neuroimmune Pharmacol.4, 462–475 (2009).
   PubMed Web of Science ®Google Scholar
• Ito T, Ito N, Saatoff M et al. Maintenance of hair follicle immune privilege is linked to prevention of NK cell attack. J. Invest. Dermatol.128, 1196–1206 (2008).
   PubMed Web of Science ®Google Scholar
• Gilhar A, Kalish RS. Alopecia areata: a tissue specific autoimmune disease of the hair follicle. Autoimmun. Rev.5, 64–69 (2006).
   PubMed Web of Science ®Google Scholar
• Gilhar A, Ullmann Y, Berkutzki T et al. Autoimmune hair loss (alopecia areata) transferred by T lymphocytes to human scalp explants on SCID mice. J. Clin. Invest.101, 62–67 (1998).
   PubMed Web of Science ®Google Scholar
• Duvic M, Welsh EA, Jackow C et al. Analysis of HLA-D locus alleles in alopecia areata patients and families. J. Invest. Dermatol.104(5 Suppl.), S5–S6 (1995).
   Google Scholar
• Colombe BW, Price VH, Khoury EL, Lou CD. HLA class II alleles in long-standing alopecia totalis/alopecia universalis and long-standing patchy alopecia areata differentiate these two clinical groups. J. Invest. Dermatol.104(5 Suppl.), S4–S5 (1995).
   Google Scholar
• Murphy GF, Lavker RM, Whitaker D, Korngold R. Cytotoxic folliculitis in GvHD: evidence of follicular stem cell injury and recovery. J. Cutan. Pathol.18, 309–314 (1990).
   Google Scholar
• Arck PC, Handjiski B, Peters EM et al. Stress inhibits hair growth in mice by induction of premature catagen development and deleterious perifollicular inflammatory events via neuropeptide substance P-dependent pathways. Am. J. Pathol.162, 803–814 (2003).
   PubMed Web of Science ®Google Scholar
• Eichmüller S, van der Veen C, Moll I et al. Clusters of perifollicular macrophages in normal murine skin: physiological degeneration of selected hair follicles by programmed organ deletion. J. Histochem. Cytochem.46, 361–370 (1998).
   PubMed Web of Science ®Google Scholar
• Pozdnyakova O, Mahalingam M. Involvement of the bulge region in primary scarring alopecia. J. Cutan. Pathol.35, 922–925 (2008).
   PubMedGoogle Scholar
• Al-Refu K, Edwards S, Ingham E, Goodfield M. Hair follicle stem cells in the pathogenesis of the scarring process in cutaneous lupus erythematosus. Presented at: Second International Conference on Cutaneous Lupus Erythematosus. Kyoto, Japan, 11–13 May, 2008.
   Google Scholar
• Kossard S. Postmenopausal frontal fibrosing alopecia. Scarring alopecia in a pattern distribution. Arch. Dermatol.130, 770–774 (1994).
   PubMedGoogle Scholar
• Kossard S, Lee MS, Wilkinson B. Postmenopausal frontal fibrosing alopecia: a frontal variant of lichen planopilaris. J. Am. Acad. Dermatol.36, 59–66 (1997).
   PubMed Web of Science ®Google Scholar
• Cotsarelis G, Millar SE. Towards a molecular understanding of hair loss and its treatment. Trends Mol. Med.7, 293–301 (2001).
   PubMed Web of Science ®Google Scholar
• Long EO. Regulation of immune responses through inhibitory receptors. Ann. Rev. Immunol.17, 875–904 (1999).
   PubMed Web of Science ®Google Scholar
• Vivier E, Tomasello E, Paul P. Lymphocyte activation via NKG2D: towards a new paradigm in immune recognition? Curr. Opin. Immunol.14, 306–311 (2002).
   PubMed Web of Science ®Google Scholar
• Bauer S, Groh V, Wu J et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science285, 727–729 (1999).
   PubMed Web of Science ®Google Scholar
• Wu J, Song Y, Bakker AB et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science285, 730–732 (1999).
   PubMed Web of Science ®Google Scholar
• King LE Jr, Mcelwee KJ, Sundburg JP. Alopecia areata. Curr. Dir. Autoimm.10, 280–312 (2008).
   PubMedGoogle Scholar
• Paus R, Eichmüller S, Hofmann U, Czarnetzki BM, Robinson P. Expression of classical and non-classical MHC class I antigens in murine hair follicles. Br. J. Dermatol.131, 177–183 (1994).
   PubMed Web of Science ®Google Scholar
• Freyschmidt-Paul P, Ziegler A, McElwee KJ et al. Treatment of alopecia areata in C3H/HeJ mice with the topical immunosuppressant FK506 (tacrolimus). Eur. J. Dermatol.11, 405–409 (2001).
   PubMed Web of Science ®Google Scholar
• Ito T, Meyer KC, Ito N, Paus R. Immune privilege and the skin. Curr. Dir. Autoimmun.10, 27–52 (2008).
   PubMedGoogle Scholar
• Ito T, Ito N, Bettermann A et al. Collapse and restoration of MHC class-I-dependent immune privilege: exploiting the human hair follicle as a model. Am. J. Pathol.164, 623–634 (2004).
   PubMed Web of Science ®Google Scholar