Wnt Signaling in Inflammation in Tissue Repair and Regeneration

Author(s): Yang Zhou, Joy Jin, Mei Feng, Di Zhu*

Journal Name: Current Protein & Peptide Science

Volume 20 , Issue 8 , 2019

Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Inflammation is the first response occurring after damage or infection, which is a defensive process for the body. It is well known that excessive inflammation can lead to further diseases such as fibrosis. But a regenerative inflammatory response can accelerate the process of repairing injury, in which a variety of cytokines, immune cells, and stem cells are involved. The Wnt signaling pathway was originally known in the field of development. Recently, its role in regenerative inflammation has gradually been established. Wnt signaling can regulate cell proliferation and differentiation through regulating participants of regenerative inflammation. Canonical and noncanonical Wnt signaling pathways are coordinated to maintain homeostasis. Based on the process of regenerative inflammation and recent research in this field, this paper reviews how the Wnt signaling pathway interact with other cells and pathways.

Keywords: Wnt signaling, inflammation, regeneration, repair, cytokines, adult stem cells, infection.

Mori, R.; Shaw, T.J.; Martin, P. Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J. Exp. Med., 2008, 205, 43-51.
Shaw, T.J.; Kishi, K.; Mori, R. Wound-associated skin fibrosis: mechanisms and treatments based on modulating the inflammatory response. Endocr. Metab. Immune Disord. Drug Targets, 2010, 10, 320-330.
Karin, M.; Clevers, H. Reparative inflammation takes charge of tissue regeneration. Nature, 2016, 529, 307-315.
Gurtner, G.C.; Werner, S.; Barrandon, Y.; Longaker, M.T. Wound repair and regeneration. Nature, 2008, 453, 314-321.
Fujiwara, N.; Kobayashi, K. Macrophages in inflammation. Curr. Drug Targets Inflamm. Allergy, 2005, 4, 281-286.
Kurimoto, T.; Yin, Y.; Habboub, G.; Gilbert, H.Y.; Li, Y.; Nakao, S.; Hafezi-Moghadam, A.; Benowitz, L.I. Neutrophils express oncomodulin and promote optic nerve regeneration. J. Neurosci., 2013, 33, 14816-14824.
Anitua, E.; Andia, I.; Ardanza, B.; Nurden, P.; Nurden, A.T. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb. Haemost., 2004, 91, 4-15.
Taniguchi, K.; Karin, M. NF-kappaB, inflammation, immunity and cancer: coming of age. Nat. Rev. Immunol., 2018, 18, 309-324.
Chen, S.E.; Jin, B.; Li, Y.P. TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am. J. Physiol. Cell Physiol., 2007, 292, C1660-C1671.
Lai, H.S.; Lin, W.H.; Lai, S.L.; Lin, H.Y.; Hsu, W.M.; Chou, C.H.; Lee, P.H. Interleukin-6 mediates angiotensinogen gene expression during liver regeneration. PLoS One, 2013, 8, e67868.
Simpson, D.M.; Ross, R. The neutrophilic leukocyte in wound repair a study with antineutrophil serum. J. Clin. Invest., 1972, 51, 2009-2023.
Pereira, C.P.; Bachli, E.B.; Schoedon, G. The wnt pathway: A macrophage effector molecule that triggers inflammation. Curr. Atheroscler. Rep., 2009, 11, 236-242.
George, S.J. Wnt pathway: A new role in regulation of inflammation. Arterioscler. Thromb. Vasc. Biol., 2008, 28, 400-402.
Kim, J.; Kim, J.; Kim, D.W.; Ha, Y.; Ihm, M.H.; Kim, H.; Song, K.; Lee, I. Wnt5a induces endothelial inflammation via beta-catenin-independent signaling. J. Immunol., 2010, 185, 1274-1282.
Stamos, J.L.; Weis, W.I. The beta-catenin destruction complex. Cold Spring Harb. Perspect. Biol., 2013, 5, a007898.
Behrens, J.; Jerchow, B.A.; Wurtele, M.; Grimm, J.; Asbrand, C.; Wirtz, R.; Kuhl, M.; Wedlich, D.; Birchmeier, W. Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science, 1998, 280, 596-599.
Rubinfeld, B.; Souza, B.; Albert, I.; Muller, O.; Chamberlain, S.H.; Masiarz, F.R.; Munemitsu, S.; Polakis, P. Association of the APC gene product with beta-catenin. Science, 1993, 262, 1731-1734.
Rubinfeld, B.; Albert, I.; Porfiri, E.; Fiol, C.; Munemitsu, S.; Polakis, P. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science, 1996, 272, 1023-1026.
Liu, C.; Li, Y.; Semenov, M.; Han, C.; Baeg, G.H.; Tan, Y.; Zhang, Z.; Lin, X.; He, X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell, 2002, 108, 837-847.
Hsu, W.; Zeng, L.; Costantini, F. Identification of a domain of Axin that binds to the serine/threonine protein phosphatase 2A and a self-binding domain. J. Biol. Chem., 1999, 274, 3439-3445.
Hart, M.; Concordet, J.P.; Lassot, I.; Albert, I.; Del, L.S.R.; Durand, H.; Perret, C.; Rubinfeld, B.; Margottin, F.; Benarous, R.; Polakis, P. The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr. Biol., 1999, 9, 207-210.
Kimelman, D.; Xu, W. Beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene, 2006, 25, 7482-7491.
Klingensmith, J.; Nusse, R.; Perrimon, N. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. Genes Dev., 1994, 8, 118-130.
Suryawanshi, A.; Tadagavadi, R.K.; Swafford, D.; Manicassamy, S. Modulation of inflammatory responses by Wnt/beta-catenin signaling in dendritic cells: A novel immunotherapy target for autoimmunity and cancer. Front. Immunol., 2016, 7, 460.
Katoh, M.; Katoh, M. WNT signaling pathway and stem cell signaling network. Clin. Cancer Res., 2007, 13, 4042-4045.
Nakamura, Y.; de Paiva, A.E.; Veenstra, G.J.; Hoppler, S. Tissue- and stage-specific Wnt target gene expression is controlled subsequent to beta-catenin recruitment to cis-regulatory modules. Development, 2016, 143, 1914-1925.
Semenov, M.V.; Habas, R.; Macdonald, B.T.; He, X. SnapShot: Noncanonical Wnt signaling pathways. Cell, 2007, 131, 1378.
De, A. Wnt/Ca2+ signaling pathway: A brief overview. Acta Biochim. Biophys. Sin. (Shanghai), 2011, 43, 745-756.
Fuster, J.J.; Zuriaga, M.A.; Ngo, D.T.; Farb, M.G.; Aprahamian, T.; Yamaguchi, T.P.; Gokce, N.; Walsh, K. Noncanonical Wnt signaling promotes obesity-induced adipose tissue inflammation and metabolic dysfunction independent of adipose tissue expansion. Diabetes, 2015, 64, 1235-1248.
Baarsma, H.A.; Skronska-Wasek, W.; Mutze, K.; Ciolek, F.; Wagner, D.E.; John-Schuster, G.; Heinzelmann, K.; Gunther, A.; Bracke, K.R.; Dagouassat, M.; Boczkowski, J.; Brusselle, G.G.; Smits, R.; Eickelberg, O.; Yildirim, A.O.; Konigshoff, M. Correction: Noncanonical WNT-5A signaling impairs endogenous lung repair in COPD. J. Exp. Med., 2017, 214, 565.
Bovolenta, P.; Rodriguez, J.; Esteve, P. Frizzled/RYK mediated signalling in axon guidance. Development, 2006, 133, 4399-4408.
Schambony, A.; Wedlich, D. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev. Cell, 2007, 12, 779-792.
Bianchi, M.E. DAMPs, PAMPs and alarmins: All we need to know about danger. J. Leukoc. Biol., 2007, 81, 1-5.
Rock, K.L.; Latz, E.; Ontiveros, F.; Kono, H. The sterile inflammatory response. Annu. Rev. Immunol., 2010, 28, 321-342.
Matzinger, P. The danger model: A renewed sense of self. Science, 2002, 296, 301-305.
Kaczmarek, A.; Vandenabeele, P.; Krysko, D.V. Necroptosis: The release of damage-associated molecular patterns and its physiological relevance. Immunity, 2013, 38, 209-223.
Kono, H.; Rock, K.L. How dying cells alert the immune system to danger. Nat. Rev. Immunol., 2008, 8, 279-289.
Tauriello, D.V.; Haegebarth, A.; Kuper, I.; Edelmann, M.J.; Henraat, M.; Canninga-van, D.M.; Kessler, B.M.; Clevers, H.; Maurice, M.M. Loss of the tumor suppressor CYLD enhances Wnt/beta-catenin signaling through K63-linked ubiquitination of Dvl. Mol. Cell, 2010, 37, 607-619.
Yuan, J.; Kroemer, G. Alternative cell death mechanisms in development and beyond. Genes Dev., 2010, 24, 2592-2602.
Krysko, O.; Vandenabeele, P.; Krysko, D.V.; Bachert, C. Impairment of phagocytosis of apoptotic cells and its role in chronic airway diseases. Apoptosis, 2010, 15, 1137-1146.
Kono, H.; Rock, K.L. How dying cells alert the immune system to danger. Nat. Rev. Immunol., 2008, 8, 279-289.
Famili, F.; Perez, L.G.; Naber, B.A.; Noordermeer, J.N.; Fradkin, L.G.; Staal, F.J. The non-canonical Wnt receptor Ryk regulates hematopoietic stem cell repopulation in part by controlling proliferation and apoptosis. Cell Death Dis., 2016, 7, e2479.
Kato, Y.; Naiki, Y.; Komatsu, T.; Takahashi, K.; Nakamura, J.; Koide, N. A Wnt pathway activator induces apoptosis and cell death in mouse monocytic leukemia cells. Oncol. Res., 2017, 25, 479-483.
Suknuntha, K.; Thita, T.; Togarrati, P.P.; Ratanachamnong, P.; Wongtrakoongate, P.; Srihirun, S.; Slukvin, I.; Hongeng, S. Wnt signaling inhibitor FH535 selectively inhibits cell proliferation and potentiates imatinib-induced apoptosis in myeloid leukemia cell lines. Int. J. Hematol., 2017, 105, 196-205.
Diwanji, N.; Bergmann, A. An unexpected friend - ROS in apoptosis-induced compensatory proliferation: Implications for regeneration and cancer. Semin. Cell Dev. Biol., 2018, 80, 74-82.
Liu, W.; Xu, X.; Fan, Z.; Sun, G.; Han, Y.; Zhang, D.; Xu, L.; Wang, M.; Wang, X.; Zhang, S.; Tang, M.; Li, J.; Chai, R.; Wang, H. Wnt signaling activates TP53-induced glycolysis and apoptosis regulator and protects against cisplatin-induced spiral ganglion neuron damage in the mouse cochlea. Antioxid. Redox Signal., 2019, 30, 1389-1410.
Jiao, X.; Cai, J.; Yu, X.; Ding, X. Paracrine activation of the Wnt/beta-catenin pathway by bone marrow stem cell attenuates cisplatin-induced kidney injury. Cell. Physiol. Biochem., 2017, 44, 1980-1994.
Andersson-Sjoland, A.; Karlsson, J.C.; Rydell-Tormanen, K. ROS-induced endothelial stress contributes to pulmonary fibrosis through pericytes and Wnt signaling. Lab. Invest., 2016, 96, 206-217.
Diwanji, N.; Bergmann, A. An unexpected friend - ROS in apoptosis-induced compensatory proliferation: Implications for regeneration and cancer. Semin. Cell Dev. Biol., 2018, 80, 74-82.
Hervera, A.; De Virgiliis, F.; Palmisano, I.; Zhou, L.; Tantardini, E.; Kong, G.; Hutson, T.; Danzi, M.C.; Perry, R.B.; Santos, C.; Kapustin, A.N.; Fleck, R.A.; Del, R.J.; Carroll, T.; Lemmon, V.; Bixby, J.L.; Shah, A.M.; Fainzilber, M.; Di Giovanni, S. Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat. Cell Biol., 2018, 20, 307-319.
Sehring, I.M.; Jahn, C.; Weidinger, G. Zebrafish fin and heart: what’s special about regeneration? Curr. Opin. Genet. Dev., 2016, 40, 48-56.
Love, N.R.; Chen, Y.; Ishibashi, S.; Kritsiligkou, P.; Lea, R.; Koh, Y.; Gallop, J.L.; Dorey, K.; Amaya, E. Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration. Nat. Cell Biol., 2013, 15, 222-228.
Wynn, T.A.; Vannella, K.M. Macrophages in tissue repair, regeneration, and fibrosis. Immunity, 2016, 44, 450-462.
Wynn, T.A.; Barron, L. Macrophages: Master regulators of inflammation and fibrosis. Semin. Liver Dis., 2010, 30, 245-257.
Cosin-Roger, J.; Ortiz-Masia, D.; Calatayud, S.; Hernandez, C.; Alvarez, A.; Hinojosa, J.; Esplugues, J.V.; Barrachina, M.D. M2 macrophages activate WNT signaling pathway in epithelial cells: Relevance in ulcerative colitis. PLoS One, 2013, 8, e78128.
Boulter, L.; Govaere, O.; Bird, T.G.; Radulescu, S.; Ramachandran, P.; Pellicoro, A.; Ridgway, R.A.; Seo, S.S.; Spee, B.; Van Rooijen, N.; Sansom, O.J.; Iredale, J.P.; Lowell, S.; Roskams, T.; Forbes, S.J. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat. Med., 2012, 18, 572-579.
Lin, S.L.; Li, B.; Rao, S.; Yeo, E.J.; Hudson, T.E.; Nowlin, B.T.; Pei, H.; Chen, L.; Zheng, J.J.; Carroll, T.J.; Pollard, J.W.; McMahon, A.P.; Lang, R.A.; Duffield, J.S. Macrophage Wnt7b is critical for kidney repair and regeneration. Proc. Natl. Acad. Sci. USA, 2010, 107, 4194-4199.
Petrie, T.A.; Strand, N.S.; Yang, C.T.; Rabinowitz, J.S.; Moon, R.T. Macrophages modulate adult zebrafish tail fin regeneration. Development, 2014, 141, 2581-2591.
Saha, S.; Aranda, E.; Hayakawa, Y.; Bhanja, P.; Atay, S.; Brodin, N.P.; Li, J.; Asfaha, S.; Liu, L.; Tailor, Y.; Zhang, J.; Godwin, A.K.; Tome, W.A.; Wang, T.C.; Guha, C.; Pollard, J.W. Macrophage-derived extracellular vesicle-packaged WNTs rescue intestinal stem cells and enhance survival after radiation injury. Nat. Commun., 2016, 7, 13096.
Palevski, D.; Levin-Kotler, L.P.; Kain, D.; Naftali-Shani, N.; Landa, N.; Ben-Mordechai, T.; Konfino, T.; Holbova, R.; Molotski, N.; Rosin-Arbesfeld, R.; Lang, R.A.; Leor, J. Loss of macrophage Wnt secretion improves remodeling and function after myocardial infarction in mice. J. Am. Heart Assoc., 2017, 6, pii: e004387.
Feng, Y.; Ren, J.; Gui, Y.; Wei, W.; Shu, B.; Lu, Q.; Xue, X.; Sun, X.; He, W.; Yang, J.; Dai, C. Wnt/beta-catenin-promoted macrophage alternative activation contributes to kidney fibrosis. J. Am. Soc. Nephrol., 2018, 29, 182-193.
Driskell, R.R.; Watt, F.M. Understanding fibroblast heterogeneity in the skin. Trends Cell Biol., 2015, 25, 92-99.
Smith, R.S.; Smith, T.J.; Blieden, T.M.; Phipps, R.P. Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. Am. J. Pathol., 1997, 151, 317-322.
van Dijk, E.M.; Menzen, M.H.; Spanjer, A.I.; Middag, L.D.; Brandsma, C.A.; Gosens, R. Noncanonical WNT-5B signaling induces inflammatory responses in human lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol., 2016, 310, L1166-L1176.
Baarsma, H.A.; Skronska-Wasek, W.; Mutze, K.; Ciolek, F.; Wagner, D.E.; John-Schuster, G.; Heinzelmann, K.; Gunther, A.; Bracke, K.R.; Dagouassat, M.; Boczkowski, J.; Brusselle, G.G.; Smits, R.; Eickelberg, O.; Yildirim, A.O.; Konigshoff, M. Noncanonical WNT-5A signaling impairs endogenous lung repair in COPD. J. Exp. Med., 2017, 214, 143-163.
Xu, L.; Cui, W.H.; Zhou, W.C.; Li, D.L.; Li, L.C.; Zhao, P.; Mo, X.T.; Zhang, Z.; Gao, J. Activation of Wnt/beta-catenin signalling is required for TGF-beta/Smad2/3 signalling during myofibroblast proliferation. J. Cell. Mol. Med., 2017, 21, 1545-1554.
Mastrogiannaki, M.; Lichtenberger, B.M.; Reimer, A.; Collins, C.A.; Driskell, R.R.; Watt, F.M. Beta-catenin stabilization in skin fibroblasts causes fibrotic lesions by preventing adipocyte differentiation of the reticular dermis. J. Invest. Dermatol., 2016, 136, 1130-1142.
Zhou, D.; Fu, H.; Zhang, L.; Zhang, K.; Min, Y.; Xiao, L.; Lin, L.; Bastacky, S.I.; Liu, Y. Tubule-derived Wnts are required for fibroblast activation and kidney fibrosis. J. Am. Soc. Nephrol., 2017, 28, 2322-2336.
Rognoni, E.; Gomez, C.; Pisco, A.O.; Rawlins, E.L.; Simons, B.D.; Watt, F.M.; Driskell, R.R. Inhibition of beta-catenin signalling in dermal fibroblasts enhances hair follicle regeneration during wound healing. Development, 2016, 143, 2522-2535.
Williams, M.R.; Azcutia, V.; Newton, G.; Alcaide, P.; Luscinskas, F.W. Emerging mechanisms of neutrophil recruitment across endothelium. Trends Immunol., 2011, 32, 461-469.
Wilgus, T.A.; Roy, S.; McDaniel, J.C. Neutrophils and wound repair: Positive actions and negative reactions. Adv. Wound Care (New Rochelle), 2013, 2, 379-388.
Hiramoto, T.; Ebihara, Y.; Mizoguchi, Y.; Nakamura, K.; Yamaguchi, K.; Ueno, K.; Nariai, N.; Mochizuki, S.; Yamamoto, S.; Nagasaki, M.; Furukawa, Y.; Tani, K.; Nakauchi, H.; Kobayashi, M.; Tsuji, K. Wnt3a stimulates maturation of impaired neutrophils developed from severe congenital neutropenia patient-derived pluripotent stem cells. Proc. Natl. Acad. Sci. USA, 2013, 110, 3023-3028.
Gallagher, R.C.; Tura-Ceide, O.; Turner, M.; Barclay, R. Analysis of Wnt pathway genes during ex vivo expansion and neutrophil differentiation of umbilical-cord-blood-derived CD34 cells. Vox Sang., 2010, 98, e290-e294.
Skokowa, J.; Cario, G.; Uenalan, M.; Schambach, A.; Germeshausen, M.; Battmer, K.; Zeidler, C.; Lehmann, U.; Eder, M.; Baum, C.; Grosschedl, R.; Stanulla, M.; Scherr, M.; Welte, K. LEF-1 is crucial for neutrophil granulocytopoiesis and its expression is severely reduced in congenital neutropenia. Nat. Med., 2006, 12, 1191-1197.
Jones, H.R.; Robb, C.T.; Perretti, M.; Rossi, A.G. The role of neutrophils in inflammation resolution. Semin. Immunol., 2016, 28, 137-145.
Jung, Y.S.; Lee, H.Y.; Kim, S.D.; Park, J.S.; Kim, J.K.; Suh, P.G.; Bae, Y.S. Wnt5a stimulates chemotactic migration and chemokine production in human neutrophils. Exp. Mol. Med., 2013, 45, e27.
Zemans, R.L.; Briones, N.; Campbell, M.; McClendon, J.; Young, S.K.; Suzuki, T.; Yang, I.V.; De Langhe, S.; Reynolds, S.D.; Mason, R.J.; Kahn, M.; Henson, P.M.; Colgan, S.P.; Downey, G.P. Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc. Natl. Acad. Sci. USA, 2011, 108, 15990-15995.
Steele, B.M.; Harper, M.T.; Macaulay, I.C.; Morrell, C.N.; Perez-Tamayo, A.; Foy, M.; Habas, R.; Poole, A.W.; Fitzgerald, D.J.; Maguire, P.B. Canonical Wnt signaling negatively regulates platelet function. Proc. Natl. Acad. Sci. USA, 2009, 106, 19836-19841.
Nelson, W.J.; Nusse, R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science, 2004, 303, 1483-1487.
Albanna, E.A.; Ahmed, H.S. Circulating Dickkopf-1 in hypoxic ischemic neonates. J. Matern. Fetal Neonatal Med., 2016, 29, 2171-2175.
Voorzanger-Rousselot, N.; Goehrig, D.; Facon, T.; Clezardin, P.; Garnero, P. Platelet is a major contributor to circulating levels of Dickkopf-1: Clinical implications in patients with multiple myeloma. Br. J. Haematol., 2009, 145, 264-266.
Macaulay, I.C.; Thon, J.N.; Tijssen, M.R.; Steele, B.M.; MacDonald, B.T.; Meade, G.; Burns, P.; Rendon, A.; Salunkhe, V.; Murphy, R.P.; Bennett, C.; Watkins, N.A.; He, X.; Fitzgerald, D.J.; Italiano, J.J.; Maguire, P.B. Canonical Wnt signaling in megakaryocytes regulates proplatelet formation. Blood, 2013, 121, 188-196.
Kim, S.Y.; Kim, S.; Yun-Choi, H.S.; Jho, E.H. Wnt5a potentiates U46619-induced platelet aggregation via the PI3K/Akt pathway. Mol. Cells, 2011, 32, 333-336.
Hendrix, S.; Nitsch, R. The role of T helper cells in neuroprotection and regeneration. J. Neuroimmunol., 2007, 184, 100-112.
Kumar, P.; Thakar, M.S.; Ouyang, W.; Malarkannan, S. IL-22 from conventional NK cells is epithelial regenerative and inflammation protective during influenza infection. Mucosal Immunol., 2013, 6, 69-82.
Liu, H.; Li, D.; Zhang, Y.; Li, M. Inflammation, mesenchymal stem cells and bone regeneration. Histochem. Cell Biol., 2018, 149, 393-404.
Ouji, Y.; Yoshikawa, M.; Shiroi, A.; Ishizaka, S. Wnt-10b secreted from lymphocytes promotes differentiation of skin epithelial cells. Biochem. Biophys. Res. Commun., 2006, 342, 1063-1069.
Tassew, N.G.; Charish, J.; Shabanzadeh, A.P.; Luga, V.; Harada, H.; Farhani, N.; D’Onofrio, P.; Choi, B.; Ellabban, A.; Nickerson, P.; Wallace, V.A.; Koeberle, P.D.; Wrana, J.L.; Monnier, P.P. Exosomes mediate mobilization of autocrine wnt10b to promote axonal regeneration in the injured CNS. Cell Reports, 2017, 20, 99-111.
Zhang, Y.; Xing, Y.; Guo, H.; Ma, X.; Li, Y. Immunohistochemical study of hair follicle stem cells in regenerated hair follicles induced by Wnt10b. Int. J. Med. Sci., 2016, 13, 765-771.
Paik, D.T.; Rai, M.; Ryzhov, S.; Sanders, L.N.; Aisagbonhi, O.; Funke, M.J.; Feoktistov, I.; Hatzopoulos, A.K. Wnt10b gain-of-function improves cardiac repair by arteriole formation and attenuation of fibrosis. Circ. Res., 2015, 117, 804-816.
Staal, F.J.; Luis, T.C.; Tiemessen, M.M. WNT signalling in the immune system: WNT is spreading its wings. Nat. Rev. Immunol., 2008, 8, 581-593.
Rothenberg, E.V.; Moore, J.E.; Yui, M.A. Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol., 2008, 8, 9-21.
Staal, F.J.; Arens, R. Wnt signaling as master regulator of T-lymphocyte responses: Implications for transplant therapy. Transplantation, 2016, 100, 2584-2592.
Blaser, H.; Dostert, C.; Mak, T.W.; Brenner, D. TNF and ROS crosstalk in inflammation. Trends Cell Biol., 2016, 26, 249-261.
Akerman, P.; Cote, P.; Yang, S.Q.; McClain, C.; Nelson, S.; Bagby, G.J.; Diehl, A.M. Antibodies to tumor necrosis factor-alpha inhibit liver regeneration after partial hepatectomy. Am. J. Physiol., 1992, 263, G579-G585.
Yamada, Y.; Kirillova, I.; Peschon, J.J.; Fausto, N. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor. Proc. Natl. Acad. Sci. USA, 1997, 94, 1441-1446.
Schwartz, M.; Solomon, A.; Lavie, V.; Ben-Bassat, S.; Belkin, M.; Cohen, A. Tumor necrosis factor facilitates regeneration of injured central nervous system axons. Brain Res., 1991, 545, 334-338.
Chen, S.E.; Jin, B.; Li, Y.P. TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am. J. Physiol. Cell Physiol., 2007, 292, C1660-C1671.
Ando, K.; Kanazawa, S.; Tetsuka, T.; Ohta, S.; Jiang, X.; Tada, T.; Kobayashi, M.; Matsui, N.; Okamoto, T. Induction of Notch signaling by tumor necrosis factor in rheumatoid synovial fibroblasts. Oncogene, 2003, 22, 7796-7803.
Neerinckx, B.; Lories, R. Mechanisms, impact and prevention of pathological bone regeneration in spondyloarthritis. Curr. Opin. Rheumatol., 2017, 29, 287-292.
Kong, X.; Liu, Y.; Ye, R.; Zhu, B.; Zhu, Y.; Liu, X.; Hu, C.; Luo, H.; Zhang, Y.; Ding, Y.; Jin, Y. GSK3beta is a checkpoint for TNF-alpha-mediated impaired osteogenic differentiation of mesenchymal stem cells in inflammatory microenvironments. Biochim. Biophys. Acta, 2013, 1830, 5119-5129.
Sang, C.; Zhang, Y.; Chen, F.; Huang, P.; Qi, J.; Wang, P.; Zhou, Q.; Kang, H.; Cao, X.; Guo, L. Tumor necrosis factor alpha suppresses osteogenic differentiation of MSCs by inhibiting semaphorin 3B via Wnt/beta-catenin signaling in estrogen-deficiency induced osteoporosis. Bone, 2016, 84, 78-87.
Yeremenko, N.; Zwerina, K.; Rigter, G.; Pots, D.; Fonseca, J.E.; Zwerina, J.; Schett, G.; Baeten, D. Tumor necrosis factor and interleukin-6 differentially regulate Dkk-1 in the inflamed arthritic joint. Arthritis Rheumatol., 2015, 67, 2071-2075.
Wang, H.; Han, X.; Wittchen, E.S.; Hartnett, M.E. TNF-alpha mediates choroidal neovascularization by upregulating VEGF expression in RPE through ROS-dependent beta-catenin activation. Mol. Vis., 2016, 22, 116-128.
Nejak-Bowen, K.; Moghe, A.; Cornuet, P.; Preziosi, M.; Nagarajan, S.; Monga, S.P. Role and regulation of p65/beta-catenin association during liver injury and regeneration: A “complex” relationship. Gene Expr., 2017, 17, 219-235.
Gregorieff, A.; Liu, Y.; Inanlou, M.R.; Khomchuk, Y.; Wrana, J.L. Yap-dependent reprogramming of Lgr5(+) stem cells drives intestinal regeneration and cancer. Nature, 2015, 526, 715-718.
Clevers, H.; Loh, K.M.; Nusse, R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science, 2014, 346, 1248012.
Neurath, M.F. New targets for mucosal healing and therapy in inflammatory bowel diseases. Mucosal Immunol., 2014, 7, 6-19.
Chen, L.W.; Egan, L.; Li, Z.W.; Greten, F.R.; Kagnoff, M.F.; Karin, M. The two faces of IKK and NF-kappaB inhibition: prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat. Med., 2003, 9, 575-581.
Ma, B.; Hottiger, M.O. Crosstalk between Wnt/beta-catenin and NF-kappaB signaling pathway during inflammation. Front. Immunol., 2016, 7, 378.
Schaper, F.; Rose-John, S. Interleukin-6: Biology, signaling and strategies of blockade. Cytokine Growth Factor Rev., 2015, 26, 475-487.
Cressman, D.E.; Greenbaum, L.E.; DeAngelis, R.A.; Ciliberto, G.; Furth, E.E.; Poli, V.; Taub, R. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science, 1996, 274, 1379-1383.
Grivennikov, S.; Karin, E.; Terzic, J.; Mucida, D.; Yu, G.Y.; Vallabhapurapu, S.; Scheller, J.; Rose-John, S.; Cheroutre, H.; Eckmann, L.; Karin, M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell, 2009, 15, 103-113.
Yeremenko, N.; Zwerina, K.; Rigter, G.; Pots, D.; Fonseca, J.E.; Zwerina, J.; Schett, G.; Baeten, D. Tumor necrosis factor and interleukin-6 differentially regulate Dkk-1 in the inflamed arthritic joint. Arthritis Rheumatol., 2015, 67, 2071-2075.
Tan, X.; Behari, J.; Cieply, B.; Michalopoulos, G.K.; Monga, S.P. Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology, 2006, 131, 1561-1572.
Thompson, M.D.; Monga, S.P. WNT/beta-catenin signaling in liver health and disease. Hepatology, 2007, 45, 1298-1305.
Jeffery, V.; Goldson, A.J.; Dainty, J.R.; Chieppa, M.; Sobolewski, A. IL-6 signaling regulates small intestinal crypt homeostasis. J. Immunol., 2017, 199, 304-311.
Bollrath, J.; Phesse, T.J.; von Burstin, V.A.; Putoczki, T.; Bennecke, M.; Bateman, T.; Nebelsiek, T.; Lundgren-May, T.; Canli, O.; Schwitalla, S.; Matthews, V.; Schmid, R.M.; Kirchner, T.; Arkan, M.C.; Ernst, M.; Greten, F.R. Gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell, 2009, 15, 91-102.
Malysheva, K.; de Rooij, K.; Lowik, C.W.; Baeten, D.L.; Rose-John, S.; Stoika, R.; Korchynskyi, O. Interleukin 6/Wnt interactions in rheumatoid arthritis: Interleukin 6 inhibits Wnt signaling in synovial fibroblasts and osteoblasts. Croat. Med. J., 2016, 57, 89-98.
Dai, W.; Liu, F.; Li, C.; Lu, Y.; Lu, X.; Du, S.; Chen, Y.; Weng, D.; Chen, J. Blockade of Wnt/beta-catenin pathway aggravated silica-induced lung inflammation through tregs regulation on Th immune responses. Mediators Inflamm., 2016, 2016, 6235614.
Nikoopour, E.; Bellemore, S.M.; Singh, B. IL-22, cell regeneration and autoimmunity. Cytokine, 2015, 74, 35-42.
Lindemans, C.A.; Calafiore, M.; Mertelsmann, A.M.; O’Connor, M.H.; Dudakov, J.A.; Jenq, R.R.; Velardi, E.; Young, L.F.; Smith, O.M.; Lawrence, G.; Ivanov, J.A.; Fu, Y.Y.; Takashima, S.; Hua, G.; Martin, M.L.; O’Rourke, K.P.; Lo, Y.H.; Mokry, M.; Romera-Hernandez, M.; Cupedo, T.; Dow, L.; Nieuwenhuis, E.E.; Shroyer, N.F.; Liu, C.; Kolesnick, R.; van den Brink, M.; Hanash, A.M. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature, 2015, 528, 560-564.
Sato, T.; Vries, R.G.; Snippert, H.J.; van de Wetering, M.; Barker, N.; Stange, D.E.; van Es, J.H.; Abo, A.; Kujala, P.; Peters, P.J.; Clevers, H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 2009, 459, 262-265.
Hu, B.L.; Shi, C.; Lei, R.E.; Lu, D.H.; Luo, W.; Qin, S.Y.; Zhou, Y.; Jiang, H.X. Interleukin-22 ameliorates liver fibrosis through miR-200a/beta-catenin. Sci. Rep., 2016, 6, 36436.
Shen, H.; Zeng, B.; Wang, C.; Tang, X.; Wang, H.; Liu, W.; Yang, Z. MiR-330 inhibits IL-22-induced keratinocyte proliferation through targeting CTNNB1. Biomed. Pharmacother., 2017, 91, 803-811.
Corr, M. Wnt signaling in ankylosing spondylitis. Clin. Rheumatol., 2014, 33, 759-762.
Weathington, N.M.; Snavely, C.A.; Chen, B.B.; Zhao, J.; Zhao, Y.; Mallampalli, R.K. Glycogen synthase kinase-3beta stabilizes the interleukin (IL)-22 receptor from proteasomal degradation in murine lung epithelia. J. Biol. Chem., 2014, 289, 17610-17619.
Zheng, Y.; Danilenko, D.M.; Valdez, P.; Kasman, I.; Eastham-Anderson, J.; Wu, J.; Ouyang, W. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature, 2007, 445, 648-651.
Eun, S.Y.; Ko, Y.S.; Park, S.W.; Chang, K.C.; Kim, H.J. IL-1beta enhances vascular smooth muscle cell proliferation and migration via P2Y2 receptor-mediated RAGE expression and HMGB1 release. Vascul. Pharmacol., 2015, 72, 108-117.
Miura, M.; Zhu, H.; Rotello, R.; Hartwieg, E.A.; Yuan, J. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell, 1993, 75, 653-660.
Mailer, R.K.; Joly, A.L.; Liu, S.; Elias, S.; Tegner, J.; Andersson, J. IL-1beta promotes Th17 differentiation by inducing alternative splicing of FOXP3. Sci. Rep., 2015, 5, 14674.
Yoshida, Y.; Yamasaki, S.; Oi, K.; Kuranobu, T.; Nojima, T.; Miyaki, S.; Ida, H.; Sugiyama, E. IL-1beta enhances Wnt signal by inhibiting DKK1. Inflammation, 2018, 41, 1945-1954.
Sun, J.; Chen, J.; Cao, J.; Li, T.; Zhuang, S.; Jiang, X. IL-1betastimulated beta-catenin up-regulation promotes angiogenesis in human lung-derived mesenchymal stromal cells through a NFkappaB- dependent microRNA-433 induction.. Oncotarget, 2016, 7, 59429-59440.
Ozeki, N.; Mogi, M.; Hase, N.; Hiyama, T.; Yamaguchi, H.; Kawai, R.; Kondo, A.; Nakata, K. Wnt16 signaling is required for IL-1beta-induced matrix metalloproteinase-13-regulated proliferation of human stem cell-derived osteoblastic cells. Int. J. Mol. Sci., 2016, 17, 221.
Sonomoto, K.; Yamaoka, K.; Oshita, K.; Fukuyo, S.; Zhang, X.; Nakano, K.; Okada, Y.; Tanaka, Y. Interleukin-1beta induces differentiation of human mesenchymal stem cells into osteoblasts via the Wnt-5a/receptor tyrosine kinase-like orphan receptor 2 pathway. Arthritis Rheum., 2012, 64, 3355-3363.
Lee, J.G.; Heur, M. Interleukin-1beta-induced Wnt5a enhances human corneal endothelial cell migration through regulation of Cdc42 and RhoA. Mol. Cell. Biol., 2014, 34, 3535-3545.
Aumiller, V.; Balsara, N.; Wilhelm, J.; Gunther, A.; Konigshoff, M. WNT/beta-catenin signaling induces IL-1beta expression by alveolar epithelial cells in pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol., 2013, 49, 96-104.
Shin, Y.; Huh, Y.H.; Kim, K.; Kim, S.; Park, K.H.; Koh, J.T.; Chun, J.S.; Ryu, J.H. Low-density lipoprotein receptor-related protein 5 governs Wnt-mediated osteoarthritic cartilage destruction. Arthritis Res. Ther., 2014, 16, R37.
Haynesworth, S.E.; Goshima, J.; Goldberg, V.M.; Caplan, A.I. Characterization of cells with osteogenic potential from human marrow. Bone, 1992, 13, 81-88.
Dennis, J.E.; Merriam, A.; Awadallah, A.; Yoo, J.U.; Johnstone, B.; Caplan, A.I. A quadripotential mesenchymal progenitor cell isolated from the marrow of an adult mouse. J. Bone Miner. Res., 1999, 14, 700-709.
Barry, F.; Boynton, R.E.; Liu, B.; Murphy, J.M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: Differentiation-dependent gene expression of matrix components. Exp. Cell Res., 2001, 268, 189-200.
Makino, S.; Fukuda, K.; Miyoshi, S.; Konishi, F.; Kodama, H.; Pan, J.; Sano, M.; Takahashi, T.; Hori, S.; Abe, H.; Hata, J.; Umezawa, A.; Ogawa, S. Cardiomyocytes can be generated from marrow stromal cells in vitro. J. Clin. Invest., 1999, 103, 697-705.
Qian, L.; Saltzman, W.M. Improving the expansion and neuronal differentiation of mesenchymal stem cells through culture surface modification. Biomaterials, 2004, 25, 1331-1337.
Banas, A.; Teratani, T.; Yamamoto, Y.; Tokuhara, M.; Takeshita, F.; Quinn, G.; Okochi, H.; Ochiya, T. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology, 2007, 46, 219-228.
Ikebe, C.; Suzuki, K. Mesenchymal stem cells for regenerative therapy: Optimization of cell preparation protocols. BioMed Res. Int., 2014, 2014, 951512.
Bianco, P.; Cao, X.; Frenette, P.S.; Mao, J.J.; Robey, P.G.; Simmons, P.J.; Wang, C.Y. The meaning, the sense and the significance: Translating the science of mesenchymal stem cells into medicine. Nat. Med., 2013, 19, 35-42.
Ling, L.; Nurcombe, V.; Cool, S.M. Wnt signaling controls the fate of mesenchymal stem cells. Gene, 2009, 433, 1-7.
Zhou, S. TGF-beta regulates beta-catenin signaling and osteoblast differentiation in human mesenchymal stem cells. J. Cell. Biochem., 2011, 112, 1651-1660.
Gao, Y.; Huang, E.; Zhang, H.; Wang, J.; Wu, N.; Chen, X.; Wang, N.; Wen, S.; Nan, G.; Deng, F.; Liao, Z.; Wu, D.; Zhang, B.; Zhang, J.; Haydon, R.C.; Luu, H.H.; Shi, L.L.; He, T.C. Crosstalk between Wnt/beta-catenin and estrogen receptor signaling synergistically promotes osteogenic differentiation of mesenchymal progenitor cells. PLoS One, 2013, 8, e82436.
Lam, S.P.; Luk, J.M.; Man, K.; Ng, K.T.; Cheung, C.K.; Rose-John, S.; Lo, C.M. Activation of interleukin-6-induced glycoprotein 130/signal transducer and activator of transcription 3 pathway in mesenchymal stem cells enhances hepatic differentiation, proliferation, and liver regeneration. Liver Transpl., 2010, 16, 1195-1206.
Ye, J.S.; Su, X.S.; Stoltz, J.F.; de Isla, N.; Zhang, L. Signalling pathways involved in the process of mesenchymal stem cells differentiating into hepatocytes. Cell Prolif., 2015, 48, 157-165.
Ke, Z.; Zhou, F.; Wang, L.; Chen, S.; Liu, F.; Fan, X.; Tang, F.; Liu, D.; Zhao, G. Down-regulation of Wnt signaling could promote bone marrow-derived mesenchymal stem cells to differentiate into hepatocytes. Biochem. Biophys. Res. Commun., 2008, 367, 342-348.
Wang, C.; Zhu, H.; Sun, Z.; Xiang, Z.; Ge, Y.; Ni, C.; Luo, Z.; Qian, W.; Han, X. Inhibition of Wnt/beta-catenin signaling promotes epithelial differentiation of mesenchymal stem cells and repairs bleomycin-induced lung injury. Am. J. Physiol. Cell Physiol., 2014, 307, C234-C244.
Shi, C.; Lv, T.; Xiang, Z.; Sun, Z.; Qian, W.; Han, X. Role of Wnt/beta-catenin signaling in epithelial differentiation of lung resident mesenchymal stem cells. J. Cell. Biochem., 2015, 116, 1532-1539.
Sun, Z.; Wang, C.; Shi, C.; Sun, F.; Xu, X.; Qian, W.; Nie, S.; Han, X. Activated Wnt signaling induces myofibroblast differentiation of mesenchymal stem cells, contributing to pulmonary fibrosis. Int. J. Mol. Med., 2014, 33, 1097-1109.
Popova, A.P.; Bozyk, P.D.; Goldsmith, A.M.; Linn, M.J.; Lei, J.; Bentley, J.K.; Hershenson, M.B. Autocrine production of TGF-beta1 promotes myofibroblastic differentiation of neonatal lung mesenchymal stem cells. Am. J. Physiol. Lung Cell. Mol. Physiol., 2010, 298, L735-L743.
Liu, A.; Chen, S.; Cai, S.; Dong, L.; Liu, L.; Yang, Y.; Guo, F.; Lu, X.; He, H.; Chen, Q.; Hu, S.; Qiu, H. Wnt5a through noncanonical Wnt/JNK or Wnt/PKC signaling contributes to the differentiation of mesenchymal stem cells into type II alveolar epithelial cells in vitro. PLoS One, 2014, 9, e90229.
Karantalis, V.; Hare, J.M. Use of mesenchymal stem cells for therapy of cardiac disease. Circ. Res., 2015, 116, 1413-1430.
Amado, L.C.; Saliaris, A.P.; Schuleri, K.H.; St, J.M.; Xie, J.S.; Cattaneo, S.; Durand, D.J.; Fitton, T.; Kuang, J.Q.; Stewart, G.; Lehrke, S.; Baumgartner, W.W.; Martin, B.J.; Heldman, A.W.; Hare, J.M. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc. Natl. Acad. Sci. USA, 2005, 102, 11474-11479.
Cohen, E.D.; Tian, Y.; Morrisey, E.E. Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development, 2008, 135, 789-798.
Aisagbonhi, O.; Rai, M.; Ryzhov, S.; Atria, N.; Feoktistov, I.; Hatzopoulos, A.K. Experimental myocardial infarction triggers canonical Wnt signaling and endothelial-to-mesenchymal transition. Dis. Model. Mech., 2011, 4, 469-483.
Duan, J.; Gherghe, C.; Liu, D.; Hamlett, E.; Srikantha, L.; Rodgers, L.; Regan, J.N.; Rojas, M.; Willis, M.; Leask, A.; Majesky, M.; Deb, A. Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J., 2012, 31, 429-442.
Lamouille, S.; Xu, J.; Derynck, R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol., 2014, 15, 178-196.
Alfaro, M.P.; Pagni, M.; Vincent, A.; Atkinson, J.; Hill, M.F.; Cates, J.; Davidson, J.M.; Rottman, J.; Lee, E.; Young, P.P. The Wnt modulator sFRP2 enhances mesenchymal stem cell engraftment, granulation tissue formation and myocardial repair. Proc. Natl. Acad. Sci. USA, 2008, 105, 18366-18371.
Pardali, E.; Sanchez-Duffhues, G.; Gomez-Puerto, M.C.; Ten, D.P. TGF-beta-induced endothelial-mesenchymal transition in fibrotic diseases. Int. J. Mol. Sci., 2017, 18, E2157.
Edeling, M.; Ragi, G.; Huang, S.; Pavenstadt, H.; Susztak, K. Developmental signalling pathways in renal fibrosis: The roles of Notch, Wnt and Hedgehog. Nat. Rev. Nephrol., 2016, 12, 426-439.
van der Flier, L.G.; Clevers, H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol., 2009, 71, 241-260.
Crosnier, C.; Stamataki, D.; Lewis, J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat. Rev. Genet., 2006, 7, 349-359.
Umar, S. Intestinal stem cells. Curr. Gastroenterol. Rep., 2010, 12, 340-348.
Barker, N.; van Es, J.H.; Kuipers, J.; Kujala, P.; van den Born, M.; Cozijnsen, M.; Haegebarth, A.; Korving, J.; Begthel, H.; Peters, P.J.; Clevers, H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature, 2007, 449, 1003-1007.
de Lau, W.; Barker, N.; Low, T.Y.; Koo, B.K.; Li, V.S.; Teunissen, H.; Kujala, P.; Haegebarth, A.; Peters, P.J.; van de Wetering, M.; Stange, D.E.; van Es, J.E.; Guardavaccaro, D.; Schasfoort, R.B.; Mohri, Y.; Nishimori, K.; Mohammed, S.; Heck, A.J.; Clevers, H. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature, 2011, 476, 293-297.
Sato, T.; van Es, J.H.; Snippert, H.J.; Stange, D.E.; Vries, R.G.; van den Born, M.; Barker, N.; Shroyer, N.F.; van de Wetering, M.; Clevers, H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature, 2011, 469, 415-418.
Farin, H.F.; Van Es, J.H.; Clevers, H. Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology, 2012, 143, 1518-1529.e7.
Shoshkes-Carmel, M.; Wang, Y.J.; Wangensteen, K.J.; Toth, B.; Kondo, A.; Massasa, E.E.; Itzkovitz, S.; Kaestner, K.H. Subepithelial telocytes are an important source of Wnts that supports intestinal crypts. Nature, 2018, 557, 242-246.
Fevr, T.; Robine, S.; Louvard, D.; Huelsken, J. Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol. Cell. Biol., 2007, 27, 7551-7559.
Pinto, D.; Gregorieff, A.; Begthel, H.; Clevers, H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev., 2003, 17, 1709-1713.
Sansom, O.J.; Reed, K.R.; Hayes, A.J.; Ireland, H.; Brinkmann, H.; Newton, I.P.; Batlle, E.; Simon-Assmann, P.; Clevers, H.; Nathke, I.S.; Clarke, A.R.; Winton, D.J. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev., 2004, 18, 1385-1390.
He, X.C.; Zhang, J.; Tong, W.G.; Tawfik, O.; Ross, J.; Scoville, D.H.; Tian, Q.; Zeng, X.; He, X.; Wiedemann, L.M.; Mishina, Y.; Li, L. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat. Genet., 2004, 36, 1117-1121.
Kabiri, Z.; Greicius, G.; Zaribafzadeh, H.; Hemmerich, A.; Counter, C.M.; Virshup, D.M. Wnt signaling suppresses MAPK-driven proliferation of intestinal stem cells. J. Clin. Invest., 2018, 128, 3806-3812.
Kriz, V.; Korinek, V. Wnt, RSPO and hippo signalling in the intestine and intestinal stem cells. Genes (Basel), 2018, 9, pii: E20.
Nierhoff, D.; Ogawa, A.; Oertel, M.; Chen, Y.Q.; Shafritz, D.A. Purification and characterization of mouse fetal liver epithelial cells with high in vivo repopulation capacity. Hepatology, 2005, 42, 130-139.
Lin, F.; Cordes, K.; Li, L.; Hood, L.; Couser, W.G.; Shankland, S.J.; Igarashi, P. Hematopoietic stem cells contribute to the regeneration of renal tubules after renal ischemia-reperfusion injury in mice. J. Am. Soc. Nephrol., 2003, 14, 1188-1199.
Grant, M.B.; May, W.S.; Caballero, S.; Brown, G.A.; Guthrie, S.M.; Mames, R.N.; Byrne, B.J.; Vaught, T.; Spoerri, P.E.; Peck, A.B.; Scott, E.W. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat. Med., 2002, 8, 607-612.
Reya, T.; Duncan, A.W.; Ailles, L.; Domen, J.; Scherer, D.C.; Willert, K.; Hintz, L.; Nusse, R.; Weissman, I.L. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 2003, 423, 409-414.
Famili, F.; Brugman, M.H.; Taskesen, E.; Naber, B.; Fodde, R.; Staal, F. High levels of canonical Wnt signaling lead to loss of stemness and increased differentiation in hematopoietic stem cells. Stem Cell Reports, 2016, 6, 652-659.
Sugimura, R.; He, X.C.; Venkatraman, A.; Arai, F.; Box, A.; Semerad, C.; Haug, J.S.; Peng, L.; Zhong, X.B.; Suda, T.; Li, L. Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell, 2012, 150, 351-365.
Murdoch, B.; Chadwick, K.; Martin, M.; Shojaei, F.; Shah, K.V.; Gallacher, L.; Moon, R.T.; Bhatia, M. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc. Natl. Acad. Sci. USA, 2003, 100, 3422-3427.
Nemeth, M.J.; Topol, L.; Anderson, S.M.; Yang, Y.; Bodine, D.M. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc. Natl. Acad. Sci. USA, 2007, 104, 15436-15441.
Povinelli, B.J.; Nemeth, M.J. Wnt5a regulates hematopoietic stem cell proliferation and repopulation through the Ryk receptor. Stem Cells, 2014, 32, 105-115.
Famili, F.; Perez, L.G.; Naber, B.A.; Noordermeer, J.N.; Fradkin, L.G.; Staal, F.J. The non-canonical Wnt receptor Ryk regulates hematopoietic stem cell repopulation in part by controlling proliferation and apoptosis. Cell Death Dis., 2016, 7, e2479.
Duncan, A.W.; Rattis, F.M.; DiMascio, L.N.; Congdon, K.L.; Pazianos, G.; Zhao, C.; Yoon, K.; Cook, J.M.; Willert, K.; Gaiano, N.; Reya, T. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol., 2005, 6, 314-322.
Perry, J.M.; He, X.C.; Sugimura, R.; Grindley, J.C.; Haug, J.S.; Ding, S.; Li, L. Cooperation between both Wnt/beta-catenin and PTEN/PI3K/Akt signaling promotes primitive hematopoietic stem cell self-renewal and expansion. Genes Dev., 2011, 25, 1928-1942.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Published on: 07 July, 2019
Page: [829 - 843]
Pages: 15
DOI: 10.2174/1389203720666190507094441
Price: $65

Article Metrics

PDF: 63