Chức năng của tín hiệu yếu tố tăng trưởng biến hình beta trong phát triển thận ở động vật có vú

Springer Science and Business Media LLC - Tập 36 - Trang 1663-1672 - 2020
Mihai G. Dumbrava1, Jon L. Lacanlale1,2, Christopher J. Rowan1, Norman D. Rosenblum1,2,3,4,5
1Program in Developmental and Stem Cell Biology, The Hospital for Sick Children, Toronto, Canada
2Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Canada
3Department of Physiology, University of Toronto, Toronto, Canada
4Department of Paediatrics, University of Toronto, Toronto, Canada
5Division of Nephrology, The Hospital for Sick Children, Toronto, Canada

Tóm tắt

Tín hiệu yếu tố tăng trưởng biến hình beta (TGFβ) bất thường trong quá trình phát triển phôi thai được cho là liên quan đến các bất thường bẩm sinh nghiêm trọng, bao gồm các biến dạng thận. Tuy nhiên, các cơ chế phân tử liên quan đến các biến dạng thận bẩm sinh liên quan đến tín hiệu TGFβ vẫn chưa được hiểu rõ. Ở đây, chúng tôi xem xét các hiểu biết hiện tại về các vai trò đặc hiệu cho dòng tế bào của tín hiệu TGFβ trong quá trình phát triển thận và cách mà việc điều chỉnh sai tín hiệu TGFβ góp phần vào cơ chế bệnh sinh của biến dạng thận.

Từ khóa

#TGFβ #tín hiệu yếu tố tăng trưởng biến hình #phát triển thận #bệnh sinh #bất thường bẩm sinh

Tài liệu tham khảo

Scott RP, Quaggin SE (2015) The cell biology of renal filtration. J Cell Biol 209:199–210 McMahon AP (2016) Development of the mammalian kidney. Curr Top Dev Biol 117:31–64 Taguchi A, Kaku Y, Ohmori T, Sharmin S, Ogawa M, Sasaki H, Nishinakamura R (2014) Redefining the in vivo origin of metanephric nephron progenitors enables generation of complex kidney structures from pluripotent stem cells. Cell Stem Cell 14:53–67 Takasato M, Little MH (2015) The origin of the mammalian kidney: Implications for recreating the kidney in vitro. Dev 142:1937–1947 Little MH, Combes AN, Takasato M (2016) Understanding kidney morphogenesis to guide renal tissue regeneration. Nat Rev Nephrol 12:624–635 Blake J, Rosenblum ND (2014) Renal branching morphogenesis: morphogenetic and signaling mechanisms. Semin Cell Dev Biol 36:2–12 Costantini F, Kopan R (2010) Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18:698–712 Mugford JW, Sipilä P, McMahon JA, McMahon AP (2008) Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev Biol 324:88–98 Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3:169–181 Kobayashi A, Mugford JW, Krautzberger AM, Naiman N, Liao J, McMahon AP (2014) Identification of a multipotent self-renewing stromal progenitor population during mammalian kidney organogenesis. Stem Cell Reports 3:650–662 O’Brien LL, McMahon AP (2014) Induction and patterning of the metanephric nephron. Semin Cell Dev Biol 36:31–38 Li W, Hartwig S, Rosenblum ND (2014) Developmental origins and functions of stromal cells in the normal and diseased mammalian kidney. Dev Dyn 243:853–863 Descargues P, Sil AK, Sano Y, Korchynskyi O, Han G, Owens P, Wang XJ, Karin M (2008) IKKα is a critical coregulator of a Smad4-independent TGFβ-Smad2/3 signaling pathway that controls keratinocyte differentiation. Proc Natl Acad Sci U S A 105:2487–2492 Muraoka RS, Dumont N, Ritterr CA, Dugger TC, Brantley DM, Chen J, Easterly E, Roebuck LR, Ryan S, Gotwals PJ, Koteliansky V, Arteaga CL (2002) Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest 109:1551–1559 Tomlinson DC, Freestone SH, Grace OC, Thomson AA (2004) Differential effects of transforming growth factor-β1 on cellular proliferation in the developing prostate. Endocrinology 145:4292–4300 Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ (1995) Defective haematopoiesis and vasculogenesis in transforming growth factor-β1 knock out mice. Development 121:1845–1854 Oshima M, Oshima H, Taketo MM (1996) TGF-β receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 179:297–302 Azhar M, Schultz JEJ, Grupp I, Dorn GW II, Meneton P, Molin DGM, Gittenberger-de Groot AC, Doetschman T (2003) Transforming growth factor beta in cardiovascular development and function. Cytokine Growth Factor Rev 14:391–407 Shull MM, Ormsby I, Kier AB, Kier AB, Pawlowskr S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvint D, Annunziata N, Doetschman T (1992) Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359:693–699 Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM, Karlsson S (1993) Transforming growth factor β1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 90:770–774 Oxburgh L, Chu GC, Michael SK, Robertson EJ (2004) TGFβ superfamily signals are required for morphogenesis of the kidney mesenchyme progenitor population. Development 131:4593–4605 Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T (1997) TGFβ2 knockout mice have multiple developmental defects that are non-overlapping with other TGFβ knockout phenotypes. Development 124:2659–2670 Bush KT, Sakurai H, Steer DL, Leonard MO, Sampogna RV, Meyer TN, Schwesinger C, Qiao J, Nigam SK (2004) TGF-β superfamily members modulate growth, branching, shaping, and patterning of the ureteric bud. Dev Biol 266:285–298 Walker KA, Sims-Lucas S, Caruana G, Cullen-McEwen L, Li J, Sarraj MA, Bertram JF, Stenvers KL (2011) Betaglycan is required for the establishment of nephron endowment in the mouse. PLoS One 6:e18723 Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B, Ramirez F, Sakai LY, Dietz HC (2003) Dysregulation of TGF-β activation contributes to pathogenesis in Marfan syndrome. Nat Genet 33:407–411 Letarte M, McDonald ML, Li C, Kathirkamathamby K, Vera S, Pece-Barbara N, Kumar S (2005) Reduced endothelial secretion and plasma levels of transforming growth factor-β1 in patients with hereditary hemorrhagic telangiectasia type 1. Cardiovasc Res 68:155–164 Harradine KA, Akhurst RJ (2006) Mutations of TGFβ signaling molecules in human disease. Ann Med 38:403–414 Rowan CJ, Li W, Martirosyan H, Erwood S, Hu D, Kim YK, Sheybani-Deloui S, Mulder J, Blake J, Chen L, Rosenblum ND (2018) Hedgehog-GLI signaling in Foxd1-positive stromal cells promotes murine nephrogenesis via TGFβ signaling. Development 145:dev159947 Meng XM, Huang XR, Xiao J, Chen HY, Zhong X, Chung ACK, Lan HY (2012) Diverse roles of TGF-β receptor II in renal fibrosis and inflammation in vivo and in vitro. J Pathol 227:175–188 Chung ACK, Lan HY (2013) Molecular mechanisms of TGF-β signaling in renal fibrosis. Curr Pathobiol Rep 1:291–299 Schnaper HW, Hayashida T, Hubchak SC, Poncelet AC (2003) TGF-β signal transduction and mesangial cell fibrogenesis. Am J Physiol Ren Physiol 284:243–252 Shi Y, Massagué J (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113:685–700 Heldin CH, Landström M, Moustakas A (2009) Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol 21:166–176 Maeshima A, Nojima Y, Kojima I (2001) The role of the activin-follistatin system in the developmental and regeneration processes of the kidney. Cytokine Growth Factor Rev 12:289–298 Zhang YE (2009) Non-Smad pathways in TGF-β signaling. Cell Res 19:128–139 Clark AT, Young RJ, Bertram JF (2001) In vitro studies on the roles of transforming growth factor-β1 in rat metanephric development. Kidney Int 59:1641–1653 Plisov SY, Yoshino K, Dove LF, Higinbotham KG, Rubin JS, Perantoni JS (2001) TGFβ2, LIF and FGF2 cooperate to induce nephrogenesis. Development 128:1045–1057 Cooley BC, Nevado J, Mellad J, Yang D, St. Hilaire C, Negro A, Fang F, Chen G, San H, Walts AD, Schwartzbeck RL, Taylor B, Lanzer JD, Wragg A, Elagha A, Beltran LE, Berry C, Feil R, Virmani R, Ladich E, Kovacic JC, Boehm M (2014) TGF-β signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling. Sci Transl Med 6:227ra34 Combes AN, Phipson B, Lawlor KT, Dorison A, Patrick R, Zappia L, Harvey RP, Oshlack A, Little MH (2019) Single cell analysis of the developing mouse kidney provides deeper insight into marker gene expression and ligand-receptor crosstalk. Development 146:dev178673 Ransick A, Lindström NO, Liu J, Zhu Q, Guo JJ, Alvarado GF, Kim AD, Black HG, Kim J, McMahon AP (2019) Single-cell profiling reveals sex, lineage, and regional diversity in the mouse kidney. Dev Cell 51:399–413 Vrljicak P, Myburgh D, Ryan AK, van Rooijen MA, Mummery CL, Gupta IR (2004) Smad expression during kidney development. Am J Physiol Ren Physiol 286:625–633 Itoh S, Itoh F, Goumans MJ, Dijke PT (2000) Signaling of transforming growth factor-β family members through Smad proteins. Eur J Biochem 267:6954–6967 Blobe GC, Schiemann WP, Pepin MC, Beauchemin M, Moustakas M, Lodish HF, O’Connor-McCourt MD (2001) Functional roles for the cytoplasmic domain of the type III transforming growth factor β receptor in regulating transforming growth factor β signaling. J Biol Chem 276:24627–24637 Villarreal MM, Kim SK, Barron L, Kodali R, Baardsnes J, Hinck CS, Krzysiak TC, Henen MA, Pakhomova O, Mendoza V, O’Connor-McCourt MD (2016) Binding properties of the transforming growth factor-β coreceptor betaglycan: proposed mechanism for potentiation of receptor complex assembly and signaling. Biochemistry 55:6880–6896 Kutz SM, Hordines J, McKeown-Longo PJ, Higgins PJ (2001) TGF-β1-induced PAI-1 gene expression requires MEK activity and cell-to-substrate adhesion. J Cell Sci 114:3905–3914 Liang YY, Brunicardi FC, Lin X (2009) Smad3 mediates immediate early induction of Id1 by TGF-β. Cell Res 19:140–148 Ling MT, Wang X, Tsao SW, Wong YC (2002) Down-regulation of Id-1 expression is associated with TGFβ1-induced growth arrest in prostate epithelial cells. Biochim Biophys Acta 1570:145–152 Brodin G, Åhgren A, Ten Dijke P, Heldin CH, Heuchel R (2000) Efficient TGF-β induction of the Smad7 gene requires cooperation between AP-1, Sp1, and Smad proteins on the mouse Smad7 promoter. J Biol Chem 275:29023–29030 Afrakhte M, Morén A, Jossan S, Itoh S, Sampath K, Westermark B, Heldin CH, Heldin NE, ten Dijke P (1998) Induction of inhibitory Smad6 and Smad7 mRNA by TGF-β family members. Biochem Biophys Res Commun 249:505–511 Topper JN, Cai J, Qiu Y, Anderson KR, Xu YY, Deeds JD, Feeley R, Gimeno CJ, Woolf EA, Tayber O, Mays GG, Sampson BB, Schoen FJ, Gimbrone MA Jr, Falb D (1997) Vascular MADs: Two novel MAD-related genes selectively inducible by flow in human vascular endothelium. Proc Natl Acad Sci U S A 94:9314–9319 Han G, Lu SL, Li AG, He W, Corless CL, Kulesz-Martin M, Wang XJ (2005) Distinct mechanisms of TGF-β1-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis. J Clin Invest 115:1714–1723 Magella B, Adam M, Potter AS, Venkatasubramanian M, Chetal K, Hay SB, Salomonis N, Potter SS (2018) Cross-platform single cell analysis of kidney development shows stromal cells express Gdnf. Dev Biol 434:36–47 Menon R, Otto EA, Kokoruda A, Zhou J, Zhang Z, Yoon E, Chen YC, Troyanskaya O, Spence JR, Kretzler M, Cebrián C (2018) Single-cell analysis of progenitor cell dynamics and lineage specification in the human fetal kidney. Development 145:dev164038 Banas MC, Parks WT, Hudkins KL, Banas B, Holdren M, Iyoda M, Wietecha TA, Kowalewska J, Liu G, Alpers CE (2007) Localization of TGF-β signaling intermediates Smad2, 3, 4, and 7 in developing and mature human and mouse kidney. J Histochem Cytochem 55:275–285 Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A (1999) Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126:1631–1642 Sirard C, De La Pompa JL, Elia A, Itie A, Mirstos C, Cheung A, Hahn S, Wakeham A, Schwartz L, Kern SE, Rossant J, Make TW (1998) The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev 12:107–119 Tremblay KD, Dunn NR, Robertson EJ (2001) Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128:3609–3621 Weinstein M, Yang X, Li C, Xu X, Gotay J, Deng CX (1998) Failure of egg cylinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor smad2. Proc Natl Acad Sci U S A 95:9378–9383 Yang X, Li C, Xu X, Deng C (1998) The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc Natl Acad Sci U S A 95:3667–3672 Zhao GQ (2003) Consequences of knocking out BMP signaling in the mouse. Genesis 35:43–56 Dünker N, Krieglstein K (2002) Tgfβ2-/-Tgfβ3-/- double knockout mice display severe midline fusion defects and early embryonic lethality. Anat Embryol (Berl) 206:73–83 Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, Tabin CJ (2006) Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2:e216 Settle SH, Rountree RB, Sinha A, Thacker A, Higgins K, Kingsley DM (2003) Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol 254:116–130 Wu MY, Hill CS (2009) TGF-β superfamily signaling in embryonic development and homeostasis. Dev Cell 16:329–343 Ritvos O, Tuuri T, Erämaa M, Sainio K, Hildén K, Saxén L, Gilbert SF (1995) Activin disrupts epithelial branching morphogenesis in developing glandular organs of the mouse. Mech Dev 50:229–245 Kulkarni AB, Ward JM, Yaswen L, Mackall CL, Bauer SR, Huh CG, Gress RE, Karlsson S (1995) Transforming growth factor-β1 null mice. An animal model for inflammatory disorders. Am J Pathol 146:264–275 Boivin GP, O’Toole BA, Orsmby IE, Diebold RJ, Eis MJ, Doetschman T, Kier AB (1995) Onset and progression of pathological lesions in transforming growth factor-β1-deficient mice. Am J Pathol 146:276–288 Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J (1995) Abnormal lung development and cleft palate in mice lacking TGF–β3 indicates defects of epithelial–mesenchymal interaction. Nat Genet 11:415–421 Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, Ding J, Ferguson MWJ, Doetschman T (1995) Transforming growth factor–β3 is required for secondary palate fusion. Nat Genet 11:409–414 Pelton RW, Saxena B, Jones M, Moses HL, Gold LI (1991) Immunohistochemical localization of TGFβ1, TGFβ2, and TGFβ3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol 115:1091–1105 Sims-Lucas S, Caruana G, Dowling J, Kett MM, Bertram JF (2008) Augmented and accelerated nephrogenesis in TGF-β2 heterozygous mutant mice. Pediatr Res 63:607–612 Short KM, Hodson MJ, Smyth IM (2010) Tomographic quantification of branching morphogenesis and renal development. Kidney Int 77:1132–1139 Short K, Hodson M, Smyth I (2013) Spatial mapping and quantification of developmental branching morphogenesis. Development 140:471–478 Piscione TD, Phan T, Rosenblum ND (2001) BMP7 controls collecting tubule cell proliferation and apoptosis via Smad1-dependent and -independent pathways. Am J Physiol Ren Physiol 280:19–33 Gewin L, Bulus N, Mernaugh G, Moeckel G, Harris RC, Moses HL, Pozzi A, Zent R (2010) TGF-β receptor deletion in the renal collecting system exacerbates fibrosis. J Am Soc Nephrol 21:1334–1343 Gewin L (2019) The many talents of transforming growth factor-β in the kidney. Curr Opin Nephrol Hypertens 28:203–210 Bridgewater D, Cox B, Cain J, Lau A, Athaide V, Gill PS, Kuure S, Sainio K, Rosenblum ND (2008) Canonical WNT/β-catenin signaling is required for ureteric branching. Dev Biol 317:83–94 Liu A, Dardik A, Ballerimann BJ (1999) Neutralizing TGF-β1 antibody infusion in neonatal rat delays in vivo glomerular capillary formation. Kidney Int 56:1334–1348 Doetschman T, Georgieva T, Li H, Reed TD, Grisham C, Friel J, Estabrook MA, Gard C, Sanford LP, Azhar M (2012) Generation of mice with a conditional allele for the transforming growth factor beta3 gene. Genesis 50:59–66 Ishtiaq Ahmed AS, Bose GC, Huang L, Azhar M (2014) Generation of mice carrying a knockout-first and conditional-ready allele of transforming growth factor beta2 gene. Genesis 52:817–826 Sheybani-Deloui S, Chi L, Staite MV, Cain JE, Nieman BJ, Henkelman RM, Wainwright BJ, Potter SS, Bagli DJ, Lorenzo AJ, Rosenblum ND (2018) Activated Hedgehog-GLI signaling causes congenital ureteropelvic junction obstruction. J Am Soc Nephrol 29:532–544 Van Der Ven AT, Connaughton DM, Ityel H, Mann N, Nakayama M, Chen J, Vivante A, Hwang DY, Schulz J, Braun DA, Schmidt JM, Schapiro D, Schneider R, Warejko JK, Daga A, Majmundar AJ, Tan W, Jobst-Schwan T, Hermle T, Widmeier E, Ashraf S, Amar A, Hoogstraaten CA, Hugo H, Kitzler TM, Kause F, Kolvenbach CM, Dai R, Spaneas L, Amann K, Stein DR, Baum MA, Somers MJG, Rodig NM, Ferguson MA, Traum AZ, Daouk GH, Bogdanović R, Stajić N, Soliman NA, Kari JA, El Desoky S, Fathy HM, Milosevic D, Al-Saffar M, Awad HS, Eid LA, Selvin A, Senguttuvan P, Sanna-Cherchi S, Rehm HL, MacArthur DG, Lek M, Laricchia KM, Wilson MW, Mane SM, Lifton RP, Lee RS, Bauer SB, Lu W, Reutter HM, Tasic V, Shril S, Hildebrandt F (2018) Whole-exome sequencing identifies causative mutations in families with congenital anomalies of the kidney and urinary tract. J Am Soc Nephrol 29:2348–2361 D’Cruz R, Stronks K, Rowan CJ, Rosenblum ND (2019) Lineage-specific roles of hedgehog-GLI signaling during mammalian kidney development. Pediatr Nephrol 35:725–731