研究生: |
林鑫秀 |
---|---|
論文名稱: |
Cav3.2 T-型鈣離子通道在小鼠氣管軟骨發育的角色 The role of Cav3.2 T-type calcium channel in mouse tracheal cartilage development |
指導教授: |
李寬容
陳建璋 |
口試委員: |
顏玉庭
蘇怡璇 洪士杰 |
學位類別: |
博士 Doctor |
系所名稱: |
生命科學暨醫學院 - 分子醫學研究所 Institute of Molecular Medicine |
論文出版年: | 2014 |
畢業學年度: | 102 |
語文別: | 英文 |
論文頁數: | 75 |
中文關鍵詞: | T-型鈣離子通 、氣管 |
外文關鍵詞: | Cav3.2, Sox9, trachea |
相關次數: | 點閱:4 下載:0 |
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中文摘要
細胞內的鈣離子通透對於間葉細胞分化成軟骨細胞的初期是很重要的,但對於受電流調控活性的鈣離子通道蛋白 (voltage-gated calcium channel) 與間葉細胞(mesenchymal cell) 分化成軟骨細胞 (chondrocyte) 的機制研究,仍然不清楚。目前,我們實驗室發現,T-型鈣離子通道 (Cav3.2) 對於小鼠氣管軟骨正常生成是很重要的。Cav3.2基因缺失小鼠的呼吸道中,形成先天性的氣管狹長,原因是在發育的過程中,氣管軟骨環發育缺失所造成的現象。同時我們利用大量轉殖Cav3.2基因表現到軟骨前驅細胞株 (chondroprogenitor cell, ATDC5 cell) ,發現大量表現Cav3.2基因的軟骨前驅細胞株有促使明顯的分化軟骨形成 (chondrogenesis) 。此增強的軟骨分化現象受到T-型鈣離子通道阻斷劑和calcineurin活性抑制劑給破壞。除此,我們發現參與調控軟骨生成的主要因子Sox9蛋白質,在Cav3.2缺陷小鼠的氣管發育中,表現量比正常小鼠低。更進一步研究發現,Sox9蛋白基因的上游調控區有一個NFAT蛋白結合位置,這個結合位置與鈣離子透過Cav3.2進入細胞調控Sox9蛋白的表現有關。我們的實驗結果顯示,鈣離子經由Cav3.2進入細胞,透過活化calcineurin/NFAT蛋白的訊號傳遞路徑,調控小鼠氣管軟骨生成的過程中Sox9蛋白的表現。
Akiyama, H., Chaboissier, M.-C., Behringer, R.R., Rowitch, D.H., Schedl, A., Epstein, J.A., and de Crombrugghe, B. (2004a). Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa. Proceedings of the National Academy of Sciences of the United States of America 101, 6502-6507.
Akiyama, H., Chaboissier, M.-C., Martin, J.F., Schedl, A., and de Crombrugghe, B. (2002). The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes & Development 16, 2813-2828.
Akiyama, H., Kim, J.E., Nakashima, K., Balmes, G., Iwai, N., Deng, J.M., Zhang, Z., Martin, J.F., Behringer, R.R., Nakamura, T., et al. (2005). Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci U S A 102, 14665-14670.
Akiyama, H., Lyons, J.P., Mori-Akiyama, Y., Yang, X., Zhang, R., Zhang, Z., Deng, J.M., Taketo, M.M., Nakamura, T., Behringer, R.R., et al. (2004b). Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev 18, 1072-1087.
Archer, C.W., and Francis-West, P. (2003). The chondrocyte. The international journal of biochemistry & cell biology 35, 401-404.
Arora, R., Metzger, R.J., and Papaioannou, V.E. (2012). Multiple roles and interactions of Tbx4 and Tbx5 in development of the respiratory system. PLoS genetics 8, e1002866.
Asagiri, M., Sato, K., Usami, T., Ochi, S., Nishina, H., Yoshida, H., Morita, I., Wagner, E.F., Mak, T.W., Serfling, E., et al. (2005). Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. The Journal of experimental medicine 202, 1261-1269.
Aubin, J., Lemieux, M., Tremblay, M., Berard, J., and Jeannotte, L. (1997). Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev Biol 192, 432-445.
Baljinnyam, E., De Lorenzo, M.S., Xie, L.H., Iwatsubo, M., Chen, S., Goydos, J.S., Nowycky, M.C., and Iwatsubo, K. (2010). Exchange protein directly activated by cyclic AMP increases melanoma cell migration by a Ca2+-dependent mechanism. Cancer research 70, 5607-5617.
Berridge, M.J., Lipp, P., and Bootman, M.D. (2000). The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1, 11-21.
Bi, W., Huang, W., Whitworth, D.J., Deng, J.M., Zhang, Z., Behringer, R.R., and de Crombrugghe, B. (2001). Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci U S A 98, 6698-6703.
Bijlenga, P., Liu, J.H., Espinos, E., Haenggeli, C.A., Fischer-Lougheed, J., Bader, C.R., and Bernheim, L. (2000). T-type alpha 1H Ca2+ channels are involved in Ca2+ signaling during terminal differentiation (fusion) of human myoblasts. Proc Natl Acad Sci U S A 97, 7627-7632.
Bonen, D.K., and Schmid, T.M. (1991). Elevated extracellular calcium concentrations induce type X collagen synthesis in chondrocyte cultures. The Journal of cell biology 115, 1171-1178.
Bonvin, E., Le Rouzic, P., Bernaudin, J.F., Cottart, C.H., Vandebrouck, C., Crie, A., Leal, T., Clement, A., and Bonora, M. (2008). Congenital tracheal malformation in cystic fibrosis transmembrane conductance regulator-deficient mice. The Journal of physiology 586, 3231-3243.
Bradley, E.W., and Drissi, M.H. (2010). WNT5A Regulates Chondrocyte Differentiation through Differential Use of the CaN/NFAT and IKK/NF-κB Pathways. Molecular Endocrinology 24, 1581-1593.
Carbone, E., and Lux, H.D. (1984). A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature 310, 501-502.
Carbone, E., and Lux, H.D. (1987). Single low-voltage-activated calcium channels in chick and rat sensory neurones. The Journal of physiology 386, 571-601.
Cardoso, W.V., and Lu, J. (2006). Regulation of early lung morphogenesis: questions, facts and controversies. Development 133, 1611-1624.
Catterall, W.A., Perez-Reyes, E., Snutch, T.P., and Striessnig, J. (2005). International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacological reviews 57, 411-425.
Chen, C.C., Lamping, K.G., Nuno, D.W., Barresi, R., Prouty, S.J., Lavoie, J.L., Cribbs, L.L., England, S.K., Sigmund, C.D., Weiss, R.M., et al. (2003). Abnormal coronary function in mice deficient in alpha1H T-type Ca2+ channels. Science 302, 1416-1418.
Chen, P., Carrington, J.L., Paralkar, V.M., Pierce, G.F., and Reddi, A.H. (1992). Chick limb bud mesodermal cell chondrogenesis: inhibition by isoforms of platelet-derived growth factor and reversal by recombinant bone morphogenetic protein. Experimental cell research 200, 110-117.
Chiang, C.S., Huang, C.H., Chieng, H., Chang, Y.T., Chang, D., Chen, J.J., Chen, Y.C., Chen, Y.H., Shin, H.S., Campbell, K.P., et al. (2009). The Ca(v)3.2 T-type Ca(2+) channel is required for pressure overload-induced cardiac hypertrophy in mice. Circulation research 104, 522-530.
Colter, D.C., Piera-Velazquez, S., Hawkins, D.F., Whitecavage, M.K., Jimenez, S.A., and Stokes, D.G. (2005). Regulation of the human Sox9 promoter by the CCAAT-binding factor. Matrix biology : journal of the International Society for Matrix Biology 24, 185-197.
DeLise, A.M., and Tuan, R.S. (2000). Electroporation-mediated DNA transfection of embryonic chick limb mesenchymal cells. Methods Mol Biol 137, 377-382.
Delise, A.M., and Tuan, R.S. (2002). Analysis of N-cadherin function in limb mesenchymal chondrogenesis in vitro. Developmental dynamics : an official publication of the American Association of Anatomists 225, 195-204.
Egusa, H., Doi, M., Saeki, M., Fukuyasu, S., Akashi, Y., Yokota, Y., Yatani, H., and Kamisaki, Y. (2011). The small molecule harmine regulates NFATc1 and Id2 expression in osteoclast progenitor cells. Bone 49, 264-274.
Eikenberry,E.F. and Bruckner,P. (1999). Supromolecular structure of cartilage matrix. In Dynamics of bone and cartilage metabolism, M.J.Seibel, S.P.Robins, and J.P.bilezikian, eds. (California: Academic Press,USA.), pp. 289-300.
Elluru, R.G., and Whitsett, J.A. (2004). Potential role of Sox9 in patterning tracheal cartilage ring formation in an embryonic mouse model. Archives of otolaryngology--head & neck surgery 130, 732-736.
Enomoto-Iwamoto, M., Nakamura, T., Aikawa, T., Higuchi, Y., Yuasa, T., Yamaguchi, A., Nohno, T., Noji, S., Matsuya, T., Kurisu, K., et al. (2000). Hedgehog proteins stimulate chondrogenic cell differentiation and cartilage formation. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 15, 1659-1668.
Ertel, E.A., Campbell, K.P., Harpold, M.M., Hofmann, F., Mori, Y., Perez-Reyes, E., Schwartz, A., Snutch, T.P., Tanabe, T., Birnbaumer, L., et al. (2000). Nomenclature of voltage-gated calcium channels. Neuron 25, 533-535.
Eswarakumar, V.P., Horowitz, M.C., Locklin, R., Morriss-Kay, G.M., and Lonai, P. (2004). A gain-of-function mutation of Fgfr2c demonstrates the roles of this receptor variant in osteogenesis. Proc Natl Acad Sci U S A 101, 12555-12560.
Fatt, P., and Katz, B. (1953). The electrical properties of crustacean muscle fibres. The Journal of physiology 120, 171-204.
Faust, R.A., Stroh, B., and Rimell, F. (1998). The near complete tracheal ring deformity. International journal of pediatric otorhinolaryngology 45, 171-176.
Foster, J.W., Dominguez-Steglich, M.A., Guioli, S., Kwok, C., Weller, P.A., Stevanovic, M., Weissenbach, J., Mansour, S., Young, I.D., Goodfellow, P.N., et al. (1994). Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372, 525-530.
Furtado, L.V., Putnam, A.R., Viskochil, D.H., Lowichik, A., Erickson, L.K., Dries, D.C., and Opitz, J.M. (2011). Unilateral sclerocornea and tracheal stenosis: unusual findings in a patient with Goldenhar anomaly. Fetal and pediatric pathology 30, 397-404.
Geduspan, J.S., and Solursh, M. (1993). Effects of the mesonephros and insulin-like growth factor I on chondrogenesis of limb explants. Dev Biol 156, 500-508.
Giordano, J., Prior, H.M., Bamforth, J.S., and Walter, M.A. (2001). Genetic study of SOX9 in a case of campomelic dysplasia. American journal of medical genetics 98, 176-181.
Hagiwara, S. (1975). Ca-dependent action potential. Membranes 3, 359-381.
Hakansson, C.H., Mercke, U., Sonesson, B., and Toremalm, N.G. (1976). Functional anatomy of the musculature of the trachea. Acta morphologica Neerlando-Scandinavica 14, 291-297.
Hasaniya, N., elZein, C.F., Mara, S., Barth, M.J., and Ilbawi, M. (2006). Alternative approach to the surgical management of congenital tracheal stenosis. The Annals of thoracic surgery 82, 2305-2307.
Hdud, I.M., El-Shafei, A.A., Loughna, P., Barrett-Jolley, R., and Mobasheri, A. (2012). Expression of Transient Receptor Potential Vanilloid (TRPV) Channels in Different Passages of Articular Chondrocytes. International journal of molecular sciences 13, 4433-4445.
Henick, D.H. (1993). Three-dimensional analysis of murine laryngeal development. The Annals of otology, rhinology & laryngology Supplement 159, 3-24.
Hinoi, E., Bialek, P., Chen, Y.T., Rached, M.T., Groner, Y., Behringer, R.R., Ornitz, D.M., and Karsenty, G. (2006). Runx2 inhibits chondrocyte proliferation and hypertrophy through its expression in the perichondrium. Genes Dev 20, 2937-2942.
Hockstein, N.G., McDonald-McGinn, D., Zackai, E., Bartlett, S., Huff, D.S., and Jacobs, I.N. (2004). Tracheal anomalies in Pfeiffer syndrome. Archives of otolaryngology--head & neck surgery 130, 1298-1302.
Huang, C.H., Chen, Y.C., and Chen, C.C. (2013). Physical interaction between calcineurin and Cav3.2 T-type Ca2+ channel modulates their functions. FEBS letters 587, 1723-1730.
Huang, Z., Xu, H., and Sandell, L. (2004). Negative regulation of chondrocyte differentiation by transcription factor AP-2alpha. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 19, 245-255.
Iwamoto, M., Higuchi, Y., Enomoto-Iwamoto, M., Kurisu, K., Koyama, E., Yeh, H., Rosenbloom, J., and Pacifici, M. (2001). The role of ERG (ets related gene) in cartilage development. Osteoarthritis and cartilage / OARS, Osteoarthritis Research Society 9 Suppl A, S41-47.
Jin, E.J., Choi, Y.A., Kyun Park, E., Bang, O.S., and Kang, S.S. (2007). MMP-2 functions as a negative regulator of chondrogenic cell condensation via down-regulation of the FAK-integrin beta1 interaction. Dev Biol 308, 474-484.
Kanai, Y., and Koopman, P. (1999). Structural and functional characterization of the mouse Sox9 promoter: implications for campomelic dysplasia. Human molecular genetics 8, 691-696.
Kawakami, Y., Rodriguez-Leon, J., and Izpisua Belmonte, J.C. (2006). The role of TGFbetas and Sox9 during limb chondrogenesis. Current opinion in cell biology 18, 723-729.
Kawano, S., Shoji, S., Ichinose, S., Yamagata, K., Tagami, M., and Hiraoka, M. (2002). Characterization of Ca(2+) signaling pathways in human mesenchymal stem cells. Cell calcium 32, 165-174.
Keja, J.A., Stoof, J.C., and Kits, K.S. (1991). Voltage-activated currents through calcium channels in rat pituitary melanotrophic cells. Neuroendocrinology 53, 349-359.
Kobayashi, T., and Kronenberg, H. (2005). Minireview: transcriptional regulation in development of bone. Endocrinology 146, 1012-1017.
Kronenberg, H.M. (2003). Developmental regulation of the growth plate. Nature 423, 332-336.
Lefebvre, V., and de Crombrugghe, B. (1998). Toward understanding SOX9 function in chondrocyte differentiation. Matrix biology : journal of the International Society for Matrix Biology 16, 529-540.
Lefebvre, V., Huang, W., Harley, V.R., Goodfellow, P.N., and de Crombrugghe, B. (1997). SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Molecular and Cellular Biology 17, 2336-2346.
Li, B.C., Hogue, J., Eilers, M., Mehrotra, P., Hyland, J., Holm, T., Prosen, T., and Slavotinek, A.M. (2013). Clinical report: Two patients with atelosteogenesis type I caused by missense mutations affecting the same FLNB residue. American journal of medical genetics Part A 161A, 619-625.
Li, M., Li, C., Liu, Y.H., Xing, Y., Hu, L., Borok, Z., Kwong, K.Y., and Minoo, P. (2008). Mesodermal deletion of transforming growth factor-beta receptor II disrupts lung epithelial morphogenesis: cross-talk between TGF-beta and Sonic hedgehog pathways. The Journal of biological chemistry 283, 36257-36264.
Llinas, R., Sugimori, M., Lin, J.W., and Cherksey, B. (1989). Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc Natl Acad Sci U S A 86, 1689-1693.
Llinas, R., and Yarom, Y. (1981). Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. The Journal of physiology 315, 549-567.
Magee, J.C., and Johnston, D. (1995). Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. The Journal of physiology 487 ( Pt 1), 67-90.
Mahlapuu, M., Enerback, S., and Carlsson, P. (2001). Haploinsufficiency of the forkhead gene Foxf1, a target for sonic hedgehog signaling, causes lung and foregut malformations. Development 128, 2397-2406.
Mancilla, E.E., Galindo, M., Fertilio, B., Herrera, M., Salas, K., Gatica, H., and Goecke, A. (2007). L-type calcium channels in growth plate chondrocytes participate in endochondral ossification. Journal of cellular biochemistry 101, 389-398.
Martin, J.F., Bradley, A., and Olson, E.N. (1995). The paired-like homeo box gene MHox is required for early events of skeletogenesis in multiple lineages. Genes Dev 9, 1237-1249.
Matsumoto, T., and Shindo, H. (2005). [Roles of BMP in chondrogenesis]. Nihon rinsho Japanese journal of clinical medicine 63 Suppl 10, 422-425.
Matsuo, K., Galson, D.L., Zhao, C., Peng, L., Laplace, C., Wang, K.Z., Bachler, M.A., Amano, H., Aburatani, H., Ishikawa, H., et al. (2004). Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. The Journal of biological chemistry 279, 26475-26480.
Matta, C., Fodor, J., Miosge, N., Takacs, R., Juhasz, T., Rybaltovszki, H., Toth, A., Csernoch, L., and Zakany, R. (2014). Purinergic signalling is required for calcium oscillations in migratory chondrogenic progenitor cells. Pflugers Archiv : European journal of physiology.
Matta, C., Fodor, J., Szijgyarto, Z., Juhasz, T., Gergely, P., Csernoch, L., and Zakany, R. (2008). Cytosolic free Ca2+ concentration exhibits a characteristic temporal pattern during in vitro cartilage differentiation: a possible regulatory role of calcineurin in Ca-signalling of chondrogenic cells. Cell calcium 44, 310-323.
McElreavey, K., and Fellous, M. (1997). Sex-determining genes. Trends in endocrinology and metabolism: TEM 8, 342-346.
Mendelsohn, C., Lohnes, D., Decimo, D., Lufkin, T., LeMeur, M., Chambon, P., and Mark, M. (1994). Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120, 2749-2771.
Michigami, T. (2013). Regulatory mechanisms for the development of growth plate cartilage. Cellular and molecular life sciences : CMLS 70, 4213-4221.
Miller, L.A., Wert, S.E., Clark, J.C., Xu, Y., Perl, A.K., and Whitsett, J.A. (2004). Role of Sonic hedgehog in patterning of tracheal-bronchial cartilage and the peripheral lung. Developmental dynamics : an official publication of the American Association of Anatomists 231, 57-71.
Minoo, P., Su, G., Drum, H., Bringas, P., and Kimura, S. (1999). Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev Biol 209, 60-71.
Mori-Akiyama, Y., Akiyama, H., Rowitch, D.H., and de Crombrugghe, B. (2003). Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc Natl Acad Sci U S A 100, 9360-9365.
Morishita, M., Kishino, T., Furukawa, K., Yonekura, A., Miyazaki, Y., Kanematsu, T., Yamashita, S., and Tsukazaki, T. (2001). A 30-base-pair element in the first intron of SOX9 acts as an enhancer in ATDC5. Biochemical and biophysical research communications 288, 347-355.
Murakami, S., Kan, M., McKeehan, W.L., and de Crombrugghe, B. (2000). Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 97, 1113-1118.
Muramatsu, S., Wakabayashi, M., Ohno, T., Amano, K., Ooishi, R., Sugahara, T., Shiojiri, S., Tashiro, K., Suzuki, Y., Nishimura, R., et al. (2007). Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. The Journal of biological chemistry 282, 32158-32167.
Murtaugh, L.C., Chyung, J.H., and Lassar, A.B. (1999). Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13, 225-237.
Ng, L.J., Wheatley, S., Muscat, G.E., Conway-Campbell, J., Bowles, J., Wright, E., Bell, D.M., Tam, P.P., Cheah, K.S., and Koopman, P. (1997). SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 183, 108-121.
Nowycky, M.C., Fox, A.P., and Tsien, R.W. (1985). Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316, 440-443.
Oberlender, S.A., and Tuan, R.S. (1994). Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 120, 177-187.
Park, J., Zhang, J.J., Moro, A., Kushida, M., Wegner, M., and Kim, P.C. (2010). Regulation of Sox9 by Sonic Hedgehog (Shh) is essential for patterning and formation of tracheal cartilage. Developmental dynamics : an official publication of the American Association of Anatomists 239, 514-526.
Perez-Reyes, E. (2006). Molecular characterization of T-type calcium channels. Cell calcium 40, 89-96.
Perl, A.K., Wert, S.E., Nagy, A., Lobe, C.G., and Whitsett, J.A. (2002). Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc Natl Acad Sci U S A 99, 10482-10487.
Peterson, R.E., Hoffman, S., and Kern, M.J. (2005). Opposing roles of two isoforms of the Prx1 homeobox gene in chondrogenesis. Developmental dynamics : an official publication of the American Association of Anatomists 233, 811-821.
Piera-Velazquez, S., Hawkins, D.F., Whitecavage, M.K., Colter, D.C., Stokes, D.G., and Jimenez, S.A. (2007). Regulation of the human SOX9 promoter by Sp1 and CREB. Experimental cell research 313, 1069-1079.
Que, J., Choi, M., Ziel, J.W., Klingensmith, J., and Hogan, B.L.M. (2006). Morphogenesis of the trachea and esophagus: current players and new roles for noggin and Bmps. Differentiation 74, 422-437.
Que, J., Luo, X., Schwartz, R.J., and Hogan, B.L. (2009). Multiple roles for Sox2 in the developing and adult mouse trachea. Development 136, 1899-1907.
Rajagopal, J., Carroll, T.J., Guseh, J.S., Bores, S.A., Blank, L.J., Anderson, W.J., Yu, J., Zhou, Q., McMahon, A.P., and Melton, D.A. (2008). Wnt7b stimulates embryonic lung growth by coordinately increasing the replication of epithelium and mesenchyme. Development 135, 1625-1634.
Randall, A., and Tsien, R.W. (1995). Pharmacological dissection of multiple types of Ca2+ channel currents in rat cerebellar granule neurons. The Journal of neuroscience : the official journal of the Society for Neuroscience 15, 2995-3012.
Regnier, C.H., Masson, R., Kedinger, V., Textoris, J., Stoll, I., Chenard, M.P., Dierich, A., Tomasetto, C., and Rio, M.C. (2002). Impaired neural tube closure, axial skeleton malformations, and tracheal ring disruption in TRAF4-deficient mice. Proc Natl Acad Sci U S A 99, 5585-5590.
Reinhold, M.I., Kapadia, R.M., Liao, Z., and Naski, M.C. (2006). The Wnt-inducible transcription factor Twist1 inhibits chondrogenesis. The Journal of biological chemistry 281, 1381-1388.
Rock, J.R., Futtner, C.R., and Harfe, B.D. (2008). The transmembrane protein TMEM16A is required for normal development of the murine trachea. Developmental Biology 321, 141-149.
Rutter, M.J., Vijayasekaran, S., Salamone, F.N., Cohen, A.P., Manning, P., Collins, M.H., and Mortelliti, A. (2006). Deficient tracheal rings. International journal of pediatric otorhinolaryngology 70, 1981-1984.
Saegusa, M., Hashimura, M., Suzuki, E., Yoshida, T., and Kuwata, T. (2012). Transcriptional Up-Regulation of Sox9 by NF-kappaB in Endometrial Carcinoma Cells, Modulating Cell Proliferation Through Alteration in the p14(ARF)/p53/p21(WAF1) Pathway. The American journal of pathology 181, 684-692.
Sala, F.G., Del Moral, P.M., Tiozzo, C., Alam, D.A., Warburton, D., Grikscheit, T., Veltmaat, J.M., and Bellusci, S. (2011). FGF10 controls the patterning of the tracheal cartilage rings via Shh. Development 138, 273-282.
Salter, D.M., Wright, M.O., and Millward-Sadler, S.J. (2004). NMDA receptor expression and roles in human articular chondrocyte mechanotransduction. Biorheology 41, 273-281.
Sekiya, I., Tsuji, K., Koopman, P., Watanabe, H., Yamada, Y., Shinomiya, K., Nifuji, A., and Noda, M. (2000). SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. The Journal of biological chemistry 275, 10738-10744.
Shannon, J.M., and Hyatt, B.A. (2004). Epithelial-mesenchymal interactions in the developing lung. Annual review of physiology 66, 625-645.
Shao, Y., Alicknavitch, M., and Farach-Carson, M.C. (2005). Expression of voltage sensitive calcium channel (VSCC) L-type Cav1.2 (alpha1C) and T-type Cav3.2 (alpha1H) subunits during mouse bone development. Developmental dynamics : an official publication of the American Association of Anatomists 234, 54-62.
Shiels, H., Li, X., Schumacker, P.T., Maltepe, E., Padrid, P.A., Sperling, A., Thompson, C.B., and Lindsten, T. (2000). TRAF4 deficiency leads to tracheal malformation with resulting alterations in air flow to the lungs. The American journal of pathology 157, 679-688.
Sitara, D., and Aliprantis, A.O. (2010). Transcriptional regulation of bone and joint remodeling by NFAT. Immunological reviews 233, 286-300.
Son, W.Y., Han, C.T., Lee, J.H., Jung, K.Y., Lee, H.M., and Choo, Y.K. (2002). Developmental expression patterns of alpha1H T-type Ca2+ channels during spermatogenesis and organogenesis in mice. Development, growth & differentiation 44, 181-190.
Subbarayan, V., Kastner, P., Mark, M., Dierich, A., Gorry, P., and Chambon, P. (1997). Limited specificity and large overlap of the functions of the mouse RAR gamma 1 and RAR gamma 2 isoforms. Mechanisms of development 66, 131-142.
Sudbeck, P., and Scherer, G. (1997). Two independent nuclear localization signals are present in the DNA-binding high-mobility group domains of SRY and SOX9. The Journal of biological chemistry 272, 27848-27852.
Takahata, Y., Takarada, T., Osawa, M., Hinoi, E., Nakamura, Y., and Yoneda, Y. (2008). Differential regulation of cellular maturation in chondrocytes and osteoblasts by glycine. Cell and tissue research 333, 91-103.
Tiozzo, C., De Langhe, S., Carraro, G., Alam, D.A., Nagy, A., Wigfall, C., Hajihosseini, M.K., Warburton, D., Minoo, P., and Bellusci, S. (2009). Fibroblast growth factor 10 plays a causative role in the tracheal cartilage defects in a mouse model of Apert syndrome. Pediatric research 66, 386-390.
Tomita, M., Reinhold, M.I., Molkentin, J.D., and Naski, M.C. (2002). Calcineurin and NFAT4 induce chondrogenesis. J Biol Chem, C200504200.
Tommerup, N., Schempp, W., Meinecke, P., Pedersen, S., Bolund, L., Brandt, C., Goodpasture, C., Guldberg, P., Held, K.R., Reinwein, H., et al. (1993). Assignment of an autosomal sex reversal locus (SRA1) and campomelic dysplasia (CMPD1) to 17q24.3-q25.1. Nature genetics 4, 170-174.
Tuan, R.S. (2003). Cellular signaling in developmental chondrogenesis: N-cadherin, Wnts, and BMP-2. The Journal of bone and joint surgery American volume 85-A Suppl 2, 137-141.
Tucker, G.F., Jr., Newton, L., and Ruben, R.J. (1981). Histopathology of acquired subglottic stenosis. A documented case report. The Annals of otology, rhinology, and laryngology 90, 335-338.
Tucker, J.A., and O'Rahilly, R. (1972). Observations on the embryology of the human larynx. The Annals of otology, rhinology, and laryngology 81, 520-523.
Tufan, A.C., Daumer, K.M., DeLise, A.M., and Tuan, R.S. (2002). AP-1 transcription factor complex is a target of signals from both WnT-7a and N-cadherin-dependent cell-cell adhesion complex during the regulation of limb mesenchymal chondrogenesis. Experimental cell research 273, 197-203.
Ushita, M., Saito, T., Ikeda, T., Yano, F., Higashikawa, A., Ogata, N., Chung, U., Nakamura, K., and Kawaguchi, H. (2009). Transcriptional induction of SOX9 by NF-kappaB family member RelA in chondrogenic cells. Osteoarthritis and cartilage / OARS, Osteoarthritis Research Society 17, 1065-1075.
Vermot, J., Niederreither, K., Garnier, J.M., Chambon, P., and Dolle, P. (2003). Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phenotype in newborn mice. Proc Natl Acad Sci U S A 100, 1763-1768.
Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F.D., Keutel, J., Hustert, E., et al. (1994). Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79, 1111-1120.
Wakamatsu, Y., Nomura, T., Osumi, N., and Suzuki, K. (2014). Comparative gene expression analyses reveal heterochrony for Sox9 expression in the cranial neural crest during marsupial development. Evolution & development 16, 197-206.
Wang, H., Leav, I., Ibaragi, S., Wegner, M., Hu, G.F., Lu, M.L., Balk, S.P., and Yuan, X. (2008). SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer research 68, 1625-1630.
Wang, Y., Belflower, R.M., Dong, Y.F., Schwarz, E.M., O'Keefe, R.J., and Drissi, H. (2005). Runx1/AML1/Cbfa2 mediates onset of mesenchymal cell differentiation toward chondrogenesis. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 20, 1624-1636.
Warburton, D., Schwarz, M., Tefft, D., Flores-Delgado, G., Anderson, K.D., and Cardoso, W.V. (2000). The molecular basis of lung morphogenesis. Mechanisms of development 92, 55-81.
Wilkins, B.J., Dai, Y.S., Bueno, O.F., Parsons, S.A., Xu, J., Plank, D.M., Jones, F., Kimball, T.R., and Molkentin, J.D. (2004). Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circulation research 94, 110-118.
Woods, A., Wang, G., Dupuis, H., Shao, Z., and Beier, F. (2007). Rac1 signaling stimulates N-cadherin expression, mesenchymal condensation, and chondrogenesis. The Journal of biological chemistry 282, 23500-23508.
Wright, E., Hargrave, M.R., Christiansen, J., Cooper, L., Kun, J., Evans, T., Gangadharan, U., Greenfield, A., and Koopman, P. (1995). The Sry-related gene Sox9 is expressed during chondrogenesis in mouse embryos. Nature genetics 9, 15-20.
Yoon, Y.M., Oh, C.D., Kim, D.Y., Lee, Y.S., Park, J.W., Huh, T.L., Kang, S.S., and Chun, J.S. (2000). Epidermal growth factor negatively regulates chondrogenesis of mesenchymal cells by modulating the protein kinase C-alpha, Erk-1, and p38 MAPK signaling pathways. The Journal of biological chemistry 275, 12353-12359.
Zhang, P., Jimenez, S.A., and Stokes, D.G. (2003). Regulation of human COL9A1 gene expression. Activation of the proximal promoter region by SOX9. The Journal of biological chemistry 278, 117-123.
Zhao, Q., Eberspaecher, H., Lefebvre, V., and De Crombrugghe, B. (1997). Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Developmental dynamics : an official publication of the American Association of Anatomists 209, 377-386.
Zhou, G., Lefebvre, V., Zhang, Z., Eberspaecher, H., and de Crombrugghe, B. (1998). Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo. The Journal of biological chemistry 273, 14989-14997.
Zhou, G., Zheng, Q., Engin, F., Munivez, E., Chen, Y., Sebald, E., Krakow, D., and Lee, B. (2006). Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc Natl Acad Sci U S A 103, 19004-19009.
Zuscik, M.J., Hilton, M.J., Zhang, X., Chen, D., and O'Keefe, R.J. (2008). Regulation of chondrogenesis and chondrocyte differentiation by stress. The Journal of clinical investigation 118, 429-438.