RANKL regulates differentiation of microfold cells in mouse nasopharynx-associated lymphoid tissue (NALT)

详细信息    查看全文

• 作者：Mami Mutoh ; Shunsuke Kimura ; Hiromi Takahashi-Iwanaga…
• 关键词：Microfold cells (M cells) ; Follicle ; associated epithelium ; Nasopharynx ; associated lymphoid tissue (NALT) ; Glycoprotein 2 (GP2) ; Receptor activator of nuclear factor kappa ; B ligand (RANKL)
• 刊名：Cell and Tissue Research
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：364
• 期：1
• 页码：175-184
• 全文大小：1,331 KB
• 参考文献：Asanuma H, Thompson AH, Iwasaki T, Sato Y, Inaba Y, Aizawa C, Kurata T, Tamura S (1997) Isolation and characterization of mouse nasal-associated lymphoid tissue. J Immunol Methods 202:123–131CrossRef PubMed
  Brandtzaeg P (1996) The B-cell development in tonsillar lymphoid follicles. Acta Otolaryngol Suppl 523:55–59PubMed
  Carapelli A, Regoli M, Nicoletti C, Ermini L, Fonzi L, Bertelli E (2004) Rabbit tonsil-associated M-cells express cytokeratin 20 and take up particulate antigen. J Histochem Cytochem 52:1323–1332CrossRef PubMed
  Clark MA, Jepson MA, Simmons NL, Booth TA, Hirst BH (1993) Differential expression of lectin-binding sites defines mouse intestinal M-cells. J Histochem Cytochem 41:1679–1687CrossRef PubMed
  Gebert A, Pabst R (1999) M cells at locations outside the gut. Semin Immunol 11:165–170CrossRef PubMed
  Gebert A, Willfuhr B, Pabst R (1995) The rabbit M-cell marker vimentin is present in epithelial cells of the tonsil crypt. Acta Otolaryngol 115:697–700CrossRef PubMed
  Hase K, Kawano K, Nochi T, Pontes GS, Fukuda S, Ebisawa M, Kadokura K, Tobe T, Fujimura Y, Kawano S, Yabashi A, Waguri S, Nakato G, Kimura S, Murakami T, Iimura M, Hamura K, Fukuoka S, Lowe AW, Itoh K, Kiyono H, Ohno H (2009a) Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 462:226–230CrossRef PubMed
  Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, Kitamura H, Ito M, Watarai H, Hazelett CC, Yeaman C, Ohno H (2009b) M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat Cell Biol 11:1427–1432CrossRef PubMed
  Jeong KI, Uetsuka K, Nakayama H, Doi K (1999) Glycoconjugate expression in follicle-associated epithelium (FAE) covering the nasal-associated lymphoid tissue (NALT) in specific pathogen-free and conventional rats. Exp Anim 48:23–29CrossRef PubMed
  Jepson MA, Mason CM, Bennett MK, Simmons NL, Hirst BH (1992) Co-expression of vimentin and cytokeratins in M cells of rabbit intestinal lymphoid follicle-associated epithelium. Histochem J 24:33–39CrossRef PubMed
  Kanaya T, Hase K, Takahashi D, Fukuda S, Hoshino K, Sasaki I, Hemmi H, Knoop KA, Kumar N, Sato M, Katsuno T, Yokosuka O, Toyooka K, Nakai K, Sakamoto A, Kitahara Y, Jinnohara T, McSorley SJ, Kaisho T, Williams IR, Ohno H (2012) The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells. Nat Immunol 13:729–736CrossRef PubMed PubMedCentral
  Kim DY, Sato A, Fukuyama S, Sagara H, Nagatake T, Kong IG, Goda K, Nochi T, Kunisawa J, Sato S, Yokota Y, Lee CH, Kiyono H (2011) The airway antigen sampling system: respiratory M cells as an alternative gateway for inhaled antigens. J Immunol 186:4253–4262CrossRef PubMed
  Kimura S, Muto M, Hisamoto M, Zheng M, Iwanaga T (2014) A novel type of cells expressing GP2 in the respiratory epithelium of the paranasal sinuses in mice. Biomed Res 35:329–337CrossRef PubMed
  Kimura S, Yamakami-Kimura M, Obata Y, Hase K, Kitamura H, Ohno H, Iwanaga T (2015a) Visualization of the entire differentiation process of murine M cells: suppression of their maturation in cecal patches. Mucosal Immunol 8:650–660CrossRef PubMed
  Kimura S, Kishimoto A, Mutoh M, Takahashi-Iwanaga H, Iwanaga T (2015b) GP2-expressing cells in the conjunctiva and tear ducts of mice: identification of a novel type of cells in the squamous stratified epithelium. Biomed Res 36:263–272CrossRef PubMed
  Knoop KA, Kumar N, Butler BR, Sakthivel SK, Taylor RT, Nochi T, Akiba H, Yagita H, Kiyono H, Williams IR (2009) RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J Immunol 183:5738–5747CrossRef PubMed PubMedCentral
  Kuper CF, Hameleers DM, Bruijntjes JP, Ven I van der, Biewenga J, Sminia T (1990) Lymphoid and non-lymphoid cells in nasal-associated lymphoid tissue (NALT) in the rat. An immuno- and enzyme-histochemical study. Cell Tissue Res 259:371–377
  Kuper CF, Koornstra PJ, Hameleers DM, Biewenga J, Spit BJ, Duijvestijn AM, Breda Vriesman PJ van, Sminia T (1992) The role of nasopharyngeal lymphoid tissue. Immunol Today 13:219–224
  Lau W de, Kujala P, Schneeberger K, Middendorp S, Li VS, Barker N, Martens A, Hofhuis F, DeKoter RP, Peters PJ, Nieuwenhuis E, Clevers H (2012) Peyer's patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured “miniguts”. Mol Cell Biol 32:3639–3647
  Lee JH, Kong SK, Wu ZS, Wu Q, Choe J, Cho HY, Ha SY, Kee SH, Kim YS (2010) Class II beta-tubulin is a novel marker for human tonsillar M cells and follicular dendritic cells. J Oral Pathol Med 39:533–539PubMed
  Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A (2013) Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol 6:666–677CrossRef PubMed PubMedCentral
  Nagatake T, Fukuyama S, Kim DY, Goda K, Igarashi O, Sato S, Nochi T, Sagara H, Yokota Y, Jetten AM, Kaisho T, Akira S, Mimuro H, Sasakawa C, Fukui Y, Fujihashi K, Akiyama T, Inoue J, Penninger JM, Kunisawa J, Kiyono H (2009) Id2-, RORgammat-, and LTbetaR-independent initiation of lymphoid organogenesis in ocular immunity. J Exp Med 206:2351–2364CrossRef PubMed PubMedCentral
  Nair PN, Schroeder HE (1986) Duct-associated lymphoid tissue (DALT) of minor salivary glands and mucosal immunity. Immunology 57:171–180PubMed PubMedCentral
  Ronzio RA, Kronquist KE, Lewis DS, MacDonald RJ, Mohrlok SH, O'Donnell JJ Jr (1978) Glycoprotein synthesis in the adult rat pancreas. IV. Subcellular distribution of membrane glycoproteins. Biochim Biophys Acta 508:65–84CrossRef PubMed
  Sato S, Kaneto S, Shibata N, Takahashi Y, Okura H, Yuki Y, Kunisawa J, Kiyono H (2013) Transcription factor Spi-B-dependent and -independent pathways for the development of Peyer's patch M cells. Mucosal Immunol 6:838–846CrossRef PubMed
  Stanley AC, Huntley JF, Jeffrey M, Buxton D (2001) Characterization of ovine nasal-associated lymphoid tissue and identification of M cells in the overlying follicle-associated epithelium. J Comp Pathol 125:262–270CrossRef PubMed
  Verbrugghe P, Kujala P, Waelput W, Peters PJ, Cuvelier CA (2008) Clusterin in human gut-associated lymphoid tissue, tonsils, and adenoids: localization to M cells and follicular dendritic cells. Histochem Cell Biol 129:311–320CrossRef PubMed
  Xia WF, Tang FL, Xiong L, Xiong S, Jung JU, Lee DH, Li XS, Feng X, Mei L, Xiong WC (2013) Vps35 loss promotes hyperresorptive osteoclastogenesis and osteoporosis via sustained RANKL signaling. J Cell Biol 200:821–837CrossRef PubMed PubMedCentral
  Zhao X, Sato A, Dela Cruz CS, Linehan M, Luegering A, Kucharzik T, Shirakawa AK, Marquez G, Farber JM, Williams I, Iwasaki A (2003) CCL9 is secreted by the follicle-associated epithelium and recruits dome region Peyer’s patch CD11b+ dendritic cells. J Immunol 171:2797–2803CrossRef PubMed
  
• 作者单位：Mami Mutoh (1)
  Shunsuke Kimura (2)
  Hiromi Takahashi-Iwanaga (2)
  Meri Hisamoto (3)
  Toshihiko Iwanaga (2)
  Junichiro Iida (1)
  
  1. Department of Orthodontics, Hokkaido University Graduate School of Dental Medicine, Sapporo, 060-8586, Japan
  2. Laboratory of Histology and Cytology, Hokkaido University Graduate School of Medicine, North 15, West 7, Kita-ku, Sapporo, 060-8638, Japan
  3. Division of Oral Functional Prosthodontics, Department of Oral Pathobiological Science, Hokkaido University Graduate School of Dental Medicine, Sapporo, 060-8586, Japan
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Human Genetics
  Proteomics
  Molecular Medicine
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0878

文摘

Murine nasopharynx-associated lymphoid tissue (NALT), located at the base of the nasal cavity, serves as a major site for the induction of mucosal immune responses against airway antigens. The follicle-associated epithelium (FAE) covering the luminal surface of NALT is characterized by the presence of microfold cells (M cells), which take up and transport luminal antigens to lymphocytes. Glycoprotein 2 (GP2) has recently been identified as a reliable marker for M cells in Peyer’s patches of the intestine. However, the expression of GP2 and other functional molecules in the M cells of NALT has not yet been examined. We have immunohistochemically detected GP2-expressing cells in the FAE of NALT and the simultaneous expression of other intestinal M-cell markers, namely Tnfaip2, CCL9, and Spi-B. These cells have been further identified as M cells because of their higher uptake capacity of luminal microbeads. Electron microscopic observations have shown that GP2-expressing cells on the FAE display morphological features typical of M cells: they possess short microvilli and microfolds on the luminal surface and are closely associated with intraepithelial lymphocytes. We have also found that the receptor activator of nuclear factor kappa-B ligand (RANKL) is expressed by stromal cells underneath the FAE, which provides its receptor RANK. The administration of RANKL markedly increases the number of GP2+Tnfaip2+ cells on the NALT FAE and that of intestinal M cells. These results suggest that GP2+Tnfaip2+ cells in NALT are equivalent to intestinal M cells, and that RANKL-RANK signaling induces their differentiation.