Retinoid and TGF-β Families: Crosstalk in Development, Neoplasia, Immunity, and Tissue Repair

Seminars in Nephrology

Volumn 32, Issue 3, 2012, Pages 287-294

  Xu, Qihe ^a   Kopp, Jeffrey B ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Immunology; Kidneys; Retinoic acid; Retinoic acid receptors; Retinol

Indexed keywords

CYTOKINE; FLUDARABINE; ISOPROTEIN; ISOTRETINOIN; RETINOIC ACID; RETINOID; RETINOL; RETINOL DERIVATIVE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ACNE; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; DEVELOPMENT; DISEASES; EMBRYO DEVELOPMENT; FETUS DEVELOPMENT; FIBROSIS; HUMAN; IMMUNE SYSTEM; IMMUNITY; KIDNEY DISEASE; MOLECULAR INTERACTION; NEOPLASM; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; SIGNAL TRANSDUCTION; TISSUE REPAIR;

EMBRYONIC DEVELOPMENT; FETAL DEVELOPMENT; HUMANS; NEOPLASMS; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; RETINOIDS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; TRETINOIN; VITAMIN A; WOUND HEALING;

EID: 84864124524     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2012.04.008     Document Type: Article

References (96)

1. Roberts A.B., Sporn M.B. Mechanistic interrelationships between two superfamilies: the steroid/retinoid receptors and transforming growth factor-beta. Cancer Surveys 1992, 14:205-220.
2. Xu Q., Lucio-Cazana J., Kitamura M., et al. Retinoids in nephrology: promises and pitfalls. Kidney Int 2004, 66:2119-2131.
3. Bartholin L., Powers S.E., Melhuish T.A., Lasse S., Weinstein M., Wotton D. TGIF inhibits retinoid signaling. Mol Cell Biol 2006, 26:990-1001.
4. Sheng N., Xie Z., Wang C., et al. Retinoic acid regulates bone morphogenic protein signal duration by promoting the degradation of phosphorylated Smad1. Proc Natl Acad Sci U S A 2010, 107:18886-18891.
5. Wen X., Li Y., Hu K., Dai C., Liu Y. Hepatocyte growth factor receptor signaling mediates the anti-fibrotic action of 9-cis-retinoic acid in glomerular mesangial cells. Am J Pathol 2005, 167:947-957.
6. Hoover L.L., Burton E.G., O'Neill M.L., et al. Retinoids regulate TGFbeta signaling at the level of Smad2 phosphorylation and nuclear accumulation. Biochim Biophys Acta 2008, 1783:2279-2286.
7. Cosgaya J.M., Perona R., Aranda A. Retinoic acid induces secretion of transforming growth factors by PC12 pheochromocytoma cells. Oncogene 1997, 14:579-587.
8. Dingwall M., Marchildon F., Gunanayagam A., Louis C.S., Wiper-Bergeron N. Retinoic acid-induced Smad3 expression is required for the induction of osteoblastogenesis of mesenchymal stem cells. Differentiation 2011, 82:57-65.
9. Uchida H., Kuroki M., Shitama T., Hayashi H. Activation of TGF-beta1 through up-regulation of TSP-1 by retinoic acid in retinal pigment epithelial cells. Curr Eye Res 2008, 33:199-203.
10. Singh B., Murphy R.F., Ding X.Z., et al. On the role of transforming growth factor-beta in the growth inhibitory effects of retinoic acid in human pancreatic cancer cells. Mol Cancer 2007, 6:82.
11. Xu Q., Hendry B.M., Maden M., et al. Kidneys of Alb/TGF-beta1 transgenic mice are deficient in retinoic acid and exogenous retinoic acid shows dose-dependent toxicity. Nephron Exp Nephrol 2010, 114:e127-e132.
12. Chen Y., Takeshita A., Ozaki K., Kitano S., Hanazawa S. Transcriptional regulation by transforming growth factor beta of the expression of retinoic acid and retinoid X receptor genes in osteoblastic cells is mediated through AP-1. J Biol Chem 1996, 271:31602-31606.
13. Takeuchi H., Yokota A., Ohoka Y., Iwata M. Cyp26b1 regulates retinoic acid-dependent signals in T cells and its expression is inhibited by transforming growth factor-beta. PLoS One 2011, 6:e16089.
14. Dolle P. Developmental expression of retinoic acid receptors (RARs). Nucl Recept Signal 2009, 7:e006.
15. Mark M., Ghyselinck N.B., Chambon P. Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 2009, 7:e002.
16. Moustakas A., Heldin C.H. The regulation of TGFbeta signal transduction. Development 2009, 136:3699-3714.
17. Watabe T., Miyazono K. Roles of TGF-beta family signaling in stem cell renewal and differentiation. Cell Res 2009, 19:103-115.
18. Taube J.H., Allton K., Duncan S.A., Shen L., Barton M.C. Foxa1 functions as a pioneer transcription factor at transposable elements to activate Afp during differentiation of embryonic stem cells. J Biol Chem 2010, 285:16135-16144.
19. Krueger C., Hoffmann F.M. Identification of retinoic acid in a high content screen for agents that overcome the anti-myogenic effect of TGF-beta-1. PLoS One 2010, 5:e15511.
20. Ghatpande S.K., Zhou H.R., Cakstina I., et al. Transforming growth factor beta2 is negatively regulated by endogenous retinoic acid during early heart morphogenesis. Dev Growth Differ 2010, 52:433-455.
21. Kubalak S.W., Hutson D.R., Scott K.K., Shannon R.A. Elevated transforming growth factor beta2 enhances apoptosis and contributes to abnormal outflow tract and aortic sac development in retinoic X receptor alpha knockout embryos. Development 2002, 129:733-746.
22. Li P., Pashmforoush M., Sucov H.M. Retinoic acid regulates differentiation of the secondary heart field and TGFbeta-mediated outflow tract septation. Dev Cell 2010, 18:480-485.
23. Chen F., Desai T.J., Qian J., et al. Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 2007, 134:2969-2979.
24. Chen F., Cao Y., Qian J., et al. A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J Clin Invest 2010, 120:2040-2048.
25. Colakoglu N., Kukner A. Teratogenicity of retinoic acid and its effects on TGF-beta2 expression in the developing cerebral cortex of the rat. J Mol Histol 2004, 35:823-827.
26. Colakoglu N., Kukner A., Oner J., et al. Effects of high dose retinoic acid on TGF-beta2 expression during pancreatic organogenesis. J Mol Histol 2005, 36:413-418.
27. Yu Z., Xing Y. All-trans retinoic acid inhibited chondrogenesis of mouse embryonic palate mesenchymal cells by down-regulation of TGF-beta/Smad signaling. Biochem Biophys Res Commun 2006, 340:929-934.
28. Zhang H., Li N., Tang Y., et al. Negative functional interaction of retinoic acid and TGF-beta signaling mediated by TG-interacting factor during chondrogenesis. Cell Physiol Biochem 2009, 23:157-164.
29. Butts S.C., Liu W., Li G., Frenz D.A. Transforming growth factor-beta1 signaling participates in the physiological and pathological regulation of mouse inner ear development by all-trans retinoic acid. Birth Defects Res A Clin Mol Teratol 2005, 73:218-228.
30. Preger-Ben Noon E., Barak H., Guttmann-Raviv N., Reshef R. Interplay between activin and Hox genes determines the formation of the kidney morphogenetic field. Development 2009, 136:1995-2004.
31. Wong Y.F., Kopp J.B., Roberts C., et al. Endogenous retinoic acid activity in principal cells and intercalated cells of mouse collecting duct system. PLoS One 2011, 6:e16770.
32. Gewin L., Bulus N., Mernaugh G., et al. TGF-beta receptor deletion in the renal collecting system exacerbates fibrosis. J Am Soc Nephrol 2010, 21:1334-1343.
33. Soucek K., Pachernik J., Kubala L., et al. Transforming growth factor-beta1 inhibits all-trans retinoic acid-induced apoptosis. Leuk Res 2006, 30:607-623.
34. Cao Z., Flanders K.C., Bertolette D., et al. Levels of phospho-Smad2/3 are sensors of the interplay between effects of TGF-beta and retinoic acid on monocytic and granulocytic differentiation of HL-60 cells. Blood 2003, 101:498-507.
35. Zhong H., Wang H.R., Yang S., et al. Targeting Smad4 links microRNA-146a to the TGF-beta pathway during retinoid acid induction in acute promyelocytic leukemia cell line. Int J Hematol 2010, 92:129-135.
36. Zirn B., Samans B., Spangenberg C., et al. All-trans retinoic acid treatment of Wilms tumor cells reverses expression of genes associated with high risk and relapse in vivo. Oncogene 2005, 24:5246-5251.
37. Fernandez-Calotti P., Pastor-Anglada M. All-trans-retinoic acid promotes trafficking of human concentrative nucleoside transporter-3 (hCNT3) to the plasma membrane by a TGF-beta1-mediated mechanism. J Biol Chem 2010, 285:13589-13598.
38. Tabata C., Tabata R., Hirayama N., et al. All-trans-retinoic acid inhibits tumour growth of malignant pleural mesothelioma in mice. Eur Respir J 2009, 34:1159-1167.
39. Palladino M.A., Morris R.E., Starnes H.F., Levinson A.D. The transforming growth factor-betas. A new family of immunoregulatory molecules. Ann N Y Acad Sci 1990, 593:181-187.
40. Li M.O., Flavell R.A. TGF-beta: a master of all T cell trades. Cell 2008, 134:392-404.
41. Pino-Lagos K., Guo Y., Noelle R.J. Retinoic acid: a key player in immunity. Biofactors 2010, 36:430-436.
42. Duriancik D.M., Lackey D.E., Hoag K.A. Vitamin A as a regulator of antigen presenting cells. J Nutr 2010, 140:1395-1399.
43. Mucida D., Cheroutre H. TGFbeta and retinoic acid intersect in immune-regulation. Cell Adh Migr 2007, 1:142-144.
44. Mucida D., Park Y., Cheroutre H. From the diet to the nucleus: vitamin A and TGF-beta join efforts at the mucosal interface of the intestine. Semin Immunol 2009, 21:14-21.
45. Gorelik L., Flavell R.A. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 2000, 12:171-181.
46. Shull M.M., Ormsby I., Kier A.B., et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992, 359:693-699.
47. Kulkarni A.B., Huh C.G., Becker D., et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 1993, 90:770-774.
48. Diebold R.J., Eis M.J., Yin M., et al. Early-onset multifocal inflammation in the transforming growth factor beta 1-null mouse is lymphocyte mediated. Proc Natl Acad Sci U S A 1995, 92:12215-12219.
49. Sanford L.P., Ormsby I., Gittenberger-de Groot A.C., et al. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 1997, 124:2659-2670.
50. Kaartinen V., Voncken J.W., Shuler C., et al. Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 1995, 11:415-421.
51. Marks B.R., Nowyhed H.N., Choi J.Y., et al. Thymic self-reactivity selects natural interleukin 17-producing T cells that can regulate peripheral inflammation. Nat Immunol 2009, 10:1125-1132.
52. Flavell R.A., Sanjabi S., Wrzesinski S.H., Licona-Limon P. The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 2010, 10:554-567.
53. Ooi J.D., Kitching A.R., Holdsworth S.R. Review: T helper 17 cells: their role in glomerulonephritis. Nephrology (Carlton) 2010, 15:513-521.
54. Das J., Ren G., Zhang L., et al. Transforming growth factor beta is dispensable for the molecular orchestration of Th17 cell differentiation. J Exp Med 2009, 206:2407-2416.
55. Santarlasci V., Maggi L., Capone M., et al. TGF-beta indirectly favors the development of human Th17 cells by inhibiting Th1 cells. Eur J Immunol 2009, 39:207-215.
56. Maeda H., Shiraishi A. TGF-beta contributes to the shift toward Th2-type responses through direct and IL-10-mediated pathways in tumor-bearing mice. J Immunol 1996, 156:73-78.
57. van Ginkel F.W., Wahl S.M., Kearney J.F., et al. Partial IgA-deficiency with increased Th2-type cytokines in TGF-beta 1 knockout mice. J Immunol 1999, 163:1951-1957.
58. Cazac B.B., Roes J. TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 2000, 13:443-451.
59. van Vlasselaer P., Punnonen J., de Vries J.E. Transforming growth factor-beta directs IgA switching in human B cells. J Immunol 1992, 148:2062-2067.
60. Watanabe K., Sugai M., Nambu Y., et al. Requirement for Runx proteins in IgA class switching acting downstream of TGF-beta 1 and retinoic acid signaling. J Immunol 2010, 184:2785-2792.
61. Takimoto T., Wakabayashi Y., Sekiya T., et al. Smad2 and Smad3 are redundantly essential for the TGF-beta-mediated regulation of regulatory T plasticity and Th1 development. J Immunol 2010, 185:842-855.
62. Martinez G.J., Zhang Z., Reynolds J.M., et al. Smad2 positively regulates the generation of Th17 cells. J Biol Chem 2010, 285:29039-29043.
63. Lu L., Wang J., Zhang F., et al. Role of Smad and non-Smad signals in the development of Th17 and regulatory T cells. J Immunol 2010, 184:4295-4306.
64. Pino-Lagos K., Benson M.J., Noelle R.J. Retinoic acid in the immune system. Ann N Y Acad Sci 2008, 1143:170-187.
65. Zhou X., Kong N., Wang J., et al. Cutting edge: all-trans retinoic acid sustains the stability and function of natural regulatory T cells in an inflammatory milieu. J Immunol 2010, 185:2675-2679.
66. Feng T., Cong Y., Qin H., Benveniste E.N., Elson C.O. Generation of mucosal dendritic cells from bone marrow reveals a critical role of retinoic acid. J Immunol 2010, 185:5915-5925.
67. Manicassamy S., Reizis B., Ravindran R., et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010, 329:849-853.
68. Manicassamy S., Ravindran R., Deng J., et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat Med 2009, 15:401-409.
69. Maruya M., Suzuki K., Fujimoto H., et al. Vitamin A-dependent transcriptional activation of the nuclear factor of activated T cells c1 (NFATc1) is critical for the development and survival of B1 cells. Proc Natl Acad Sci U S A 2011, 108:722-727.
70. DePaolo R.W., Abadie V., Tang F., et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature 2011, 471:220-224.
71. Stephensen C.B., Rasooly R., Jiang X., et al. Vitamin A enhances in vitro Th2 development via retinoid X receptor pathway. J Immunol 2002, 168:4495-4503.
72. Iwata M., Eshima Y., Kagechika H. Retinoic acids exert direct effects on T cells to suppress Th1 development and enhance Th2 development via retinoic acid receptors. Int Immunol 2003, 15:1017-1025.
73. Dawson H.D., Collins G., Pyle R., Key M., Taub D.D. The retinoic acid receptor-alpha mediates human T-cell activation and Th2 cytokine and chemokine production. BMC Immunol 2008, 9:16.
74. Hall J.A., Cannons J.L., Grainger J.R., et al. Essential role for retinoic acid in the promotion of CD4(+) T cell effector responses via retinoic acid receptor alpha. Immunity 2011, 34:435-447.
75. Iwata M., Hirakiyama A., Eshima Y., et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004, 21:527-538.
76. Dzhagalov I., Chambon P., He Y.W. Regulation of CD8+ T lymphocyte effector function and macrophage inflammatory cytokine production by retinoic acid receptor gamma. J Immunol 2007, 178:2113-2121.
77. Mucida D., Park Y., Kim G., et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007, 317:256-260.
78. Lu L., Zhou X., Wang J., Zheng S.G., Horwitz D.A. Characterization of protective human CD4CD25 FOXP3 regulatory T cells generated with IL-2, TGF-beta and retinoic acid. PLoS One 2010, 5:e15150.
79. Mucida D., Pino-Lagos K., Kim G., et al. Retinoic acid can directly promote TGF-beta-mediated Foxp3(+) Treg cell conversion of naive T cells. Immunity 2009, 30:471-472. reply, 472-3.
80. Kim B.S., Kim I.K., Park Y.J., et al. Conversion of Th2 memory cells into Foxp3+ regulatory T cells suppressing Th2-mediated allergic asthma. Proc Natl Acad Sci U S A 2010, 107:8742-8747.
81. Kishi M., Yasuda H., Abe Y., et al. Regulatory CD8+ T cells induced by exposure to all-trans retinoic acid and TGF-beta suppress autoimmune diabetes. Biochem Biophys Res Commun 2010, 394:228-232.
82. Lei J., Hasegawa H., Matsumoto T., Yasukawa M. Peroxisome proliferator-activated receptor alpha and gamma agonists together with TGF-beta convert human CD4+CD25- T cells into functional Foxp3+ regulatory T cells. J Immunol 2010, 185:7186-7198.
83. Xu L., Kitani A., Stuelten C., et al. Positive and negative transcriptional regulation of the Foxp3 gene is mediated by access and binding of the Smad3 protein to enhancer I. Immunity 2010, 33:313-325.
84. Suzuki K., Maruya M., Kawamoto S., et al. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010, 33:71-83.
85. Melnik B.C. Is nuclear deficiency of FoxO1 due to increased growth factor/PI3K/Akt-signalling in acne vulgaris reversed by isotretinoin treatment?. Br J Dermatol 2010, 162:1398-1400.
86. Esteban-Pretel G., Marin M.P., Renau-Piqueras J., Barber T., Timoneda J. Vitamin A deficiency alters rat lung alveolar basement membrane: reversibility by retinoic acid. J Nutr Biochem 2010, 21:227-236.
87. Liu X., Lu L., Tao B.B., Zhu Y.C. All-trans retinoic acid inhibits the increases in fibronectin and PAI-1 induced by TGF-beta1 and Ang II in rat mesangial cells. Acta Pharmacol Sin 2008, 29:1035-1041.
88. Wang H., Dan Z., Jiang H. Effect of all-trans retinoic acid on liver fibrosis induced by common bile duct ligation in rats. J Huazhong Univ Sci Technolog Med Sci 2008, 28:553-557.
89. Tanabe K., Tokuda H., Takai S., et al. Modulation by the steroid/thyroid hormone superfamily of TGF-beta-stimulated VEGF release from vascular smooth muscle cells. J Cell Biochem 2006, 99:187-195.
90. Sidell N., Feng Y., Hao L., et al. Retinoic acid is a cofactor for translational regulation of vascular endothelial growth factor in human endometrial stromal cells. Mol Endocrinol 2010, 24:148-160.
91. Glick A.B., Flanders K.C., Danielpour D., Yuspa S.H., Sporn M.B. Retinoic acid induces transforming growth factor-beta 2 in cultured keratinocytes and mouse epidermis. Cell Regul 1989, 1:87-97.
92. Jakowlew S.B., Cubert J., Danielpour D., Sporn M.B., Roberts A.B. Differential regulation of the expression of transforming growth factor-beta mRNAs by growth factors and retinoic acid in chicken embryo chondrocytes, myocytes, and fibroblasts. J Cell Physiol 1992, 150:377-385.
93. Morath C., Dechow C., Lehrke I., et al. Effects of retinoids on the TGF-beta system and extracellular matrix in experimental glomerulonephritis. J Am Soc Nephrol 2001, 12:2300-2309.
94. Morath C., Ratzlaff K., Dechow C., et al. Chronic low-dose isotretinoin treatment limits renal damage in subtotally nephrectomized rats. J Mol Med 2009, 87:53-64.
95. Kishimoto K., Kinoshita K., Hino S., et al. Therapeutic effect of retinoic acid on unilateral ureteral obstruction model. Nephron Exp Nephrol 2011, 118:e69-e78.
96. Perez de Lema G., Lucio-Cazana F.J., Molina A., et al. Retinoic acid treatment protects MRL/lpr lupus mice from the development of glomerular disease. Kidney Int 2004, 66:1018-1028.