In the past decade, researches on Wnt signaling in cell biology have made remarkable progress regarding our understanding of embryonic development, bone formation, muscle injury and repair, neurogenesis, and tumorigenesis. The study also showed that physical activity can reverse age-dependent decline in skeletal muscle, preventing osteoporosis, regenerative neurogenesis, hippocampal function, cognitive ability, and neuromuscular junction formation, and the age-dependent recession is highly correlated with Wnt signaling pathways. However, how the biological processes in cell and physical activity during/following exercise affect the Wnt signaling path of the locomotor system is largely unknown. In this study, we first briefly introduce the important features of the cellular biological processes of exercise in the locomotor system. Then, we discuss Wnt signaling and review the very few studies that have examined Wnt signaling pathways in cellular biological processes of the locomotor system during physical exercise.
Aberg E , Perlmann T , Olson L , Brene S : Running increases neurogenesis without retinoic acid receptor activation in the adult mouse dentate gyrus. Hippocampus 18, 785–792 (2008)
Albanese I , Yu B , Al-Kindi H , Barratt B , Ott L , Al-Refai M , de Varennes B , Shum-Tim D , Cerruti M , Gourgas O , Rheaume E , Tardif JC , Schwertani A : Role of noncanonical Wnt signaling pathway in human aortic valve calcification. Arterioscler. Thromb. Vasc. Biol. 37, 543–552 (2017)
Almeida M , Ambrogini E , Han L , Manolagas SC , Jilka RL : Increased lipid oxidation causes oxidative stress, increased peroxisome proliferator-activated receptor-gamma expression, and diminished pro-osteogenic Wnt signaling in the skeleton. J. Biol. Chem. 284, 27438–27448 (2009)
Amin H , Vachris J , Hamilton A , Steuerwald N , Howden R , Arthur ST : GSK3β inhibition and LEF1 upregulation in skeletal muscle following a bout of downhill running. J. Physiol. Sci. 64, 1–11 (2014)
Armstrong DD , Esser KA : Wnt/β-catenin signaling activates growth-control genes during overload-induced skeletal muscle hypertrophy. Am. J. Physiol. Cell Physiol. 289, C853–C859 (2005)
Arnsdorf EJ , Tummala P , Jacobs CR : Non-canonical Wnt signaling and N-cadherin related β-catenin signaling play a role in mechanically induced osteogenic cell fate. PLoS One 4, e5388 (2009)
Arthur ST , Cooley ID : The effect of physiological stimuli on sarcopenia; impact of Notch and Wnt signaling on impaired aged skeletal muscle repair. Int. J. Biol. Sci. 8, 731–760 (2012)
Aschenbach WG , Ho RC , Sakamoto K , Fujii N , Li Y , Kim YB , Hirshman MF , Goodyear LJ : Regulation of dishevelled and beta-catenin in rat skeletal muscle: an alternative exercise-induced GSK-3β signaling pathway. Am. J. Physiol. Endocrinol. Metab. 291, E152–158 (2006)
Baker RK , Lively MO : Purification and characterization of hen oviduct microsomal signal peptidase. Biochemistry 26, 8561–8567 (1987)
Bayod S , Mennella I , Sanchez-Roige S , Lalanza JF , Escorihuela RM , Camins A , Pallas M , Canudas AM : Wnt pathway regulation by long-term moderate exercise in rat hippocampus. Brain Res. 1543, 38–48 (2014)
Beaulieu JM , Sotnikova TD , Yao WD , Kockeritz L , Woodgett JR , Gainetdinov RR , Caron MG : Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc. Natl. Acad. Sci. U. S. A. 101, 5099–5104 (2004)
Bennell KL , Malcolm SA , Thomas SA , Reid SJ , Brukner PD , Ebeling PR , Wark JD : Risk factors for stress fractures in track and field athletes. A twelve-month prospective study. Am. J. Sports Med. 24, 810–818 (1996)
Berwick DC , Harvey K : The importance of Wnt signalling for neurodegeneration in Parkinson’s disease. Biochem. Soc. Trans. 40, 1123–1128 (2012)
Binder E , Droste SK , Ohl F , Reul JM : Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice. Behav. Brain Res. 155, 197–206 (2004)
Blotnick E , Anglister L : Exercise modulates synaptic acetylcholinesterase at neuromuscular junctions. Neuroscience 319, 221–232 (2016)
Bonewald LF , Johnson ML : Osteocytes, mechanosensing and Wnt signaling. Bone 42, 606–615 (2008)
Brack AS , Conboy MJ , Roy S , Lee M , Kuo CJ , Keller C , Rando TA : Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807–810 (2007)
Burden SJ , Yumoto N , Zhang W : The role of MuSK in synapse formation and neuromuscular disease. Cold Spring Harb. Perspect. Biol. 5, a009167 (2013)
Cabrera CV , Alonso MC , Johnston P , Phillips RG , Lawrence PA : Phenocopies induced with antisense RNA identify the wingless gene. Cell 50, 659–663 (1987)
Cadigan KM , Nusse R : Wnt signaling: a common theme in animal development. Genes Dev. 11, 3286–3305 (1997)
Cameron HA , McKay RD : Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2, 894–897 (1999)
Case N , Ma M , Sen B , Xie Z , Gross TS , Rubin J : β-Catenin levels influence rapid mechanical responses in osteoblasts. J. Biol. Chem. 283, 29196–29205 (2008)
Cavanagh PR , Licata AA , Rice AJ : Exercise and pharmacological countermeasures for bone loss during long-duration space flight. Gravit. Space Biol. Bull. 18, 39–58 (2005)
Chae WJ , Ehrlich AK , Chan PY , Teixeira AM , Henegariu O , Hao L , Shin JH , Park JH , Tang WH , Kim ST , Maher SE , Goldsmith-Pestana K , Shan P , Hwa J , Lee PJ , Krause DS , Rothlin CV , McMahon-Pratt D , Bothwell AL : The Wnt antagonist dickkopf-1 promotes pathological type 2 cell-mediated inflammation. Immunity 44, 246–258 (2016)
Charge SB , Rudnicki MA : Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209–238 (2004)
Chen J , Park CS , Tang SJ : Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J. Biol. Chem. 281, 11910–11916 (2006)
Chen M , Do H : Wnt signaling in neurogenesis during aging and physical activity. Brain Sci. 2, 745–768 (2012)
Chen X , Li L , Guo J , Zhang L , Yuan Y , Chen B , Sun Z , Xu J , Zou J : Treadmill running exercise prevents senile osteoporosis and upregulates the Wnt signaling pathway in SAMP6 mice. Oncotarget 7, 71072–71086 (2016)
Cisternas P , Inestrosa NC : Brain glucose metabolism: role of Wnt signaling in the metabolic impairment in Alzheimer’s disease. Neurosci. Biobehav. Rev. 80, 316–328 (2017)
Clevers H , Nusse R : Wnt/β-catenin signaling and disease. Cell 149, 1192–1205 (2012)
Czarkowska-Paczek B , Wesolowska K , Przybylski J : Physical exercise prevents osteoporosis. Przegl. Lek. 68, 103–106 (2011)
De Ferrari GV , Moon RT : The ups and downs of Wnt signaling in prevalent neurological disorders. Oncogene 25, 7545–7553 (2006)
Dias C , Feng J , Sun H , Shao NY , Mazei-Robison MS , Damez-Werno D , Scobie K , Bagot R , LaBonte B , Ribeiro E , Liu X , Kennedy P , Vialou V , Ferguson D , Pena C , Calipari ES , Koo JW , Mouzon E , Ghose S , Tamminga C , Neve R , Shen L , Nestler EJ : β-Catenin mediates stress resilience through Dicer1/microRNA regulation. Nature 516, 51–55 (2014)
Dimauro I , Sgura A , Pittaluga M , Magi F , Fantini C , Mancinelli R , Sgadari A , Fulle S , Caporossi D : Regular exercise participation improves genomic stability in diabetic patients: an exploratory study to analyse telomere length and DNA damage. Sci. Rep. 7, 4137 (2017)
Epp JR , Barker JM , Galea LA : Running wild: neurogenesis in the hippocampus across the lifespan in wild and laboratory-bred Norway rats. Hippocampus 19, 1040–1049 (2009)
Evans DJ , Valasek P , Schmidt C , Patel K : Skeletal muscle translocation in vertebrates. Anat. Embryol. (Berl). 211, 43–50 (2006)
Evans EM , Racette SB , Van Pelt RE , Peterson LR , Villareal DT : Effects of soy protein isolate and moderate exercise on bone turnover and bone mineral density in postmenopausal women. Menopause 14, 481–488 (2007)
Fujimaki S , Hidaka R , Asashima M , Takemasa T , Kuwabara T : Wnt protein-mediated satellite cell conversion in adult and aged mice following voluntary wheel running. J. Biol. Chem. 289, 7399–7412 (2014)
Gerenu G , Dobarro M , Ramirez MJ , Gil-Bea FJ : Early cognitive stimulation compensates for memory and pathological changes in Tg2576 mice. Biochim. Biophys. Acta 1832, 837–847 (2013)
Giles RH , van Es JH , Clevers H : Caught up in a Wnt storm: Wnt signaling in cancer. Biochim. Biophys. Acta 1653, 1–24 (2003)
Gould TD , Einat H , O’Donnell KC , Picchini AM , Schloesser RJ , Manji HK : β-Catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology 32, 2173–2183 (2007)
Hao HX , Xie Y , Zhang Y , Charlat O , Oster E , Avello M , Lei H , Mickanin C , Liu D , Ruffner H , Mao X , Ma Q , Zamponi R , Bouwmeester T , Finan PM , Kirschner MW , Porter JA , Serluca FC , Cong F : ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 485, 195–200 (2012)
Haraldstad K , Rohde G , Stea TH , Lohne-Seiler H , Hetlelid K , Paulsen G , Berntsen S : Changes in health-related quality of life in elderly men after 12 weeks of strength training. Eur. Rev. Aging Phys. Act. 14, 8 (2017)
Horii N , Uchida M , Hasegawa N , Fujie S , Oyanagi E , Yano H , Hashimoto T , Iemitsu M : Resistance training prevents muscle fibrosis and atrophy via down-regulation of C1q-induced Wnt signaling in senescent mice. FASEB J. 32, 3547–3559 (2018)
Huh JE , Ko R , Jung HJ , Lee SY : Glycogen synthase kinase 3β promotes osteogenic differentiation of murine adipose-derived stromal cells. PLoS One 8, e54551 (2013)
Inestrosa NC , Montecinos-Oliva C , Fuenzalida M : Wnt signaling: role in Alzheimer disease and schizophrenia. J. Neuroimmune Pharmacol. 7, 788–807 (2012)
Inestrosa NC , Toledo EM : The role of Wnt signaling in neuronal dysfunction in Alzheimer’s disease. Mol. Neurodegener. 3, 9 (2008)
Jing L , Lefebvre JL , Gordon LR , Granato M : Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/MuSK receptor. Neuron 61, 721–733 (2009)
Joiner DM , Ke J , Zhong Z , Xu HE , Williams BO : LRP5 and LRP6 in development and disease. Trends Endocrinol. Metab. 24, 31–39 (2013)
Kiel DP , Ferrari SL , Cupples LA , Karasik D , Manen D , Imamovic A , Herbert AG , Dupuis J : Genetic variation at the low-density lipoprotein receptor-related protein 5 (LRP5) locus modulates Wnt signaling and the relationship of physical activity with bone mineral density in men. Bone 40, 587–596 (2007)
Kim DY , Jung SY , Kim K , Kim CJ : Treadmill exercise ameliorates Alzheimer disease-associated memory loss through the Wnt signaling pathway in the streptozotocin-induced diabetic rats. J. Exerc. Rehabil. 12, 276–283 (2016)
Kim N , Burden SJ : MuSK controls where motor axons grow and form synapses. Nat. Neurosci. 11, 19–27 (2008)
Komiya Y , Habas R : Wnt signal transduction pathways. Organogenesis 4, 68–75 (2008)
Krause Neto W , Ciena AP , Anaruma CA , de Souza RR , Gama EF : Effects of exercise on neuromuscular junction components across age: systematic review of animal experimental studies. BMC Res. Notes 8, 713 (2015)
Kummer TT , Misgeld T , Sanes JR : Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr. Opin. Neurobiol. 16, 74–82 (2006)
Kurt M , Arik AC , Celik S : The effects of sertraline and fluoxetine on anxiety in the elevated plus-maze test in mice. J. Basic. Clin. Physiol. Pharmacol. 11, 173–180 (2000)
Leal ML , Lamas L , Aoki MS , Ugrinowitsch C , Ramos MS , Tricoli V , Moriscot AS : Effect of different resistance-training regimens on the WNT-signaling pathway. Eur. J. Appl. Physiol. 111, 2535–2545 (2011)
Lecker SH , Jagoe RT , Gilbert A , Gomes M , Baracos V , Bailey J , Price SR , Mitch WE , Goldberg AL : Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39–51 (2004)
Lecker SH , Solomon V , Mitch WE , Goldberg AL : Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J. Nutr. 129, 227S–237S (1999)
Li L , Chen X , Lv S , Dong M , Zhang L , Tu J , Yang J , Song Y , Xu L , Zou J : Influence of exercise on bone remodeling-related hormones and cytokines in ovariectomized rats: a model of postmenopausal osteoporosis. PLoS One 9, e112845 (2014)
Li VS , Ng SS , Boersema PJ , Low TY , Karthaus WR , Gerlach JP , Mohammed S , Heck AJ , Maurice MM , Mahmoudi T , Clevers H : Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 149, 1245–1256 (2012)
Li X , Jope RS : Is glycogen synthase kinase-3 a central modulator in mood regulation? Neuropsychopharmacology 35, 2143–2154 (2010)
Lijam N , Paylor R , McDonald MP , Crawley JN , Deng CX , Herrup K , Stevens KE , Maccaferri G , McBain CJ , Sussman DJ , Wynshaw-Boris A : Social interaction and sensorimotor gating abnormalities in mice lacking Dvl1. Cell 90, 895–905 (1997)
Lin W , Burgess RW , Dominguez B , Pfaff SL , Sanes JR , Lee KF : Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057–1064 (2001)
Liu H , Fergusson MM , Castilho RM , Liu J , Cao L , Chen J , Malide D , Rovira II , Schimel D , Kuo CJ , Gutkind JS , Hwang PM , Finkel T : Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317, 803–806 (2007)
Lorenzon A , Calore M , Poloni G , De Windt LJ , Braghetta P , Rampazzo A : Wnt/β-catenin pathway in arrhythmogenic cardiomyopathy. Oncotarget 8, 60640–60655 (2017)
Lu Y , Dong Y , Tucker D , Wang R , Ahmed ME , Brann D , Zhang Q : Treadmill exercise exerts neuroprotection and regulates microglial polarization and oxidative stress in a streptozotocin-induced rat model of sporadic Alzheimer’s disease. J. Alzheimers Dis. 56, 1469–1484 (2017)
Lustig B , Jerchow B , Sachs M , Weiler S , Pietsch T , Karsten U , van de Wetering M , Clevers H , Schlag PM , Birchmeier W , Behrens J : Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184–1193 (2002)
Mayhew DL , Kim JS , Cross JM , Ferrando AA , Bamman MM : Translational signaling responses preceding resistance training-mediated myofiber hypertrophy in young and old humans. J. Appl. Physiol. (1985) 107, 1655–1662 (2009)
Michelangeli VP , Findlay DM , Fletcher A , Martin TJ : Calcitonin gene-related peptide (CGRP) acts independently of calcitonin on cyclic AMP formation in clonal osteogenic sarcoma cells (UMR 106-01). Calcif. Tissue Int. 39, 44–48 (1986)
Mirzaei A , Zabihiyeganeh M , Jahed SA , Khiabani E , Nojomi M , Ghaffari S : Effects of vitamin D optimization on quality of life of patients with fibromyalgia: a randomized controlled trial. Med. J. Islam Repub. Iran 32, 29 (2018)
Mohammed MK , Shao C , Wang J , Wei Q , Wang X , Collier Z , Tang S , Liu H , Zhang F , Huang J , Guo D , Lu M , Liu F , Liu J , Ma C , Shi LL , Athiviraham A , He TC , Lee MJ : Wnt/β-catenin signaling plays an ever-expanding role in stem cell self-renewal, tumorigenesis and cancer chemoresistance. Genes Dis. 3, 11–40 (2016)
Naito AT , Sumida T , Nomura S , Liu ML , Higo T , Nakagawa A , Okada K , Sakai T , Hashimoto A , Hara Y , Shimizu I , Zhu W , Toko H , Katada A , Akazawa H , Oka T , Lee JK , Minamino T , Nagai T , Walsh K , Kikuchi A , Matsumoto M , Botto M , Shiojima I , Komuro I : Complement C1q activates canonical Wnt signaling and promotes aging-related phenotypes. Cell 149, 1298–1313 (2012)
Neufer PD , Dohm GL : Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle. Am. J. Physiol. Cell Physiol. 265, C1597–C1603 (1993)
Nusse R , Clevers H : Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell 169, 985–999 (2017)
Nusse R , Varmus HE : Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31, 99–109 (1982)
Okada K , Naito AT , Higo T , Nakagawa A , Shibamoto M , Sakai T , Hashimoto A , Kuramoto Y , Sumida T , Nomura S , Ito M , Yamaguchi T , Oka T , Akazawa H , Lee JK , Morimoto S , Sakata Y , Shiojima I , Komuro I : Wnt/β-catenin signaling contributes to skeletal myopathy in heart failure via direct interaction with Forkhead Box O. Circ. Heart Fail. 8, 799–808 (2015)
Okamoto H , Voleti B , Banasr M , Sarhan M , Duric V , Girgenti MJ , Dileone RJ , Newton SS , Duman RS : Wnt2 expression and signaling is increased by different classes of antidepressant treatments. Biol. Psychiatry 68, 521–527 (2010)
Okamoto M , Inoue K , Iwamura H , Terashima K , Soya H , Asashima M , Kuwabara T : Reduction in paracrine Wnt3 factors during aging causes impaired adult neurogenesis. FASEB J. 25, 3570–3582 (2011)
Otto A , Schmidt C , Luke G , Allen S , Valasek P , Muntoni F , Lawrence-Watt D , Patel K : Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J. Cell Sci. 121, 2939–2950 (2008)
Parnow A , Gharakhanlou R , Gorginkaraji Z , Rajabi S , Eslami R , Hedayati M , Mahdian R : Effects of endurance and resistance training on calcitonin gene-related peptide and acetylcholine receptor at slow and fast twitch skeletal muscles and sciatic nerve in male Wistar rats. Int. J. Pept. 2012, 962651 (2012)
Perry CG , Lally J , Holloway GP , Heigenhauser GJ , Bonen A , Spriet LL : Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J. Physiol. 588, 4795–4810 (2010)
Raab MS , Breitkreutz I , Tonon G , Zhang J , Hayden PJ , Nguyen T , Fruehauf JH , Lin BK , Chauhan D , Hideshima T , Munshi NC , Anderson KC , Podar K : Targeting PKC: a novel role for β-catenin in ER stress and apoptotic signaling. Blood 113, 1513–1521 (2009)
Redila VA , Christie BR : Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 137, 1299–1307 (2006)
Rijsewijk F , Schuermann M , Wagenaar E , Parren P , Weigel D , Nusse R : The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657 (1987)
Ruff C , Holt B , Trinkaus E : Who’s afraid of the big bad Wolff?: “Wolff’s law” and bone functional adaptation. Am. J. Phys. Anthropol. 129, 484–498 (2006)
Sakamoto K , Arnolds DE , Ekberg I , Thorell A , Goodyear LJ : Exercise regulates Akt and glycogen synthase kinase-3 activities in human skeletal muscle. Biochem. Biophys. Res. Commun. 319, 419–425 (2004)
Semenov M , Tamai K , He X : SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J. Biol. Chem. 280, 26770–26775 (2005)
Semenov MV , Habas R , Macdonald BT , He X : SnapShot: noncanonical Wnt signaling pathways. Cell 131, 1378 (2007)
Sen B , Guilluy C , Xie Z , Case N , Styner M , Thomas J , Oguz I , Rubin C , Burridge K , Rubin J : Mechanically induced focal adhesion assembly amplifies anti-adipogenic pathways in mesenchymal stem cells. Stem Cells 29, 1829–1836 (2011)
Shanely RA , Zergeroglu MA , Lennon SL , Sugiura T , Yimlamai T , Enns D , Belcastro A , Powers SK : Mechanical ventilation-induced diaphragmatic atrophy is associated with oxidative injury and increased proteolytic activity. Am. J. Respir. Crit. Care Med. 166, 1369–1374 (2002)
Sharma RP , Chopra VL : Effect of the wingless (wg1) mutation on wing and haltere development in Drosophila melanogaster. Dev. Biol. 48, 461–465 (1976)
Smith AJ , Phipps WR , Thomas W , Schmitz KH , Kurzer MS : The effects of aerobic exercise on estrogen metabolism in healthy premenopausal women. Cancer Epidemiol. Biomarkers Prev. 22, 756–764 (2013)
Spillane M , Schwarz N , Willoughby DS : Upper-body resistance exercise augments vastus lateralis androgen receptor-DNA binding and canonical Wnt/β-catenin signaling compared to lower-body resistance exercise in resistance-trained men without an acute increase in serum testosterone. Steroids 98, 63–71 (2015)
Steiner B , Kronenberg G , Jessberger S , Brandt MD , Reuter K , Kempermann G : Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46, 41–52 (2004)
Strochlic L , Falk J , Goillot E , Sigoillot S , Bourgeois F , Delers P , Rouviere J , Swain A , Castellani V , Schaeffer L , Legay C : Wnt4 participates in the formation of vertebrate neuromuscular junction. PLoS One 7, e29976 (2012)
Taipale J , Beachy PA : The Hedgehog and Wnt signalling pathways in cancer. Nature 411, 349–354 (2001)
Tew GA , Howsam J , Hardy M , Bissell L : Adapted yoga to improve physical function and health-related quality of life in physically-inactive older adults: a randomised controlled pilot trial. BMC Geriatr. 17, 131 (2017)
Tu X , Rhee Y , Condon KW , Bivi N , Allen MR , Dwyer D , Stolina M , Turner CH , Robling AG , Plotkin LI , Bellido T : Sost downregulation and local Wnt signaling are required for the osteogenic response to mechanical loading. Bone 50, 209–217 (2012)
Turner CH : Bone strength: current concepts. Ann. N Y Acad. Sci. 1068, 429–446 (2006)
Um HS , Kang EB , Koo JH , Kim HT , Jin L , Kim EJ , Yang CH , An GY , Cho IH , Cho JY : Treadmill exercise represses neuronal cell death in an aged transgenic mouse model of Alzheimer’s disease. Neurosci. Res. 69, 161–173 (2011)
van Ooyen A , Nusse R : Structure and nucleotide sequence of the putative mammary oncogene int-1; proviral insertions leave the protein-encoding domain intact. Cell 39, 233–240 (1984)
Varela-Nallar L , Inestrosa NC : Wnt signaling in the regulation of adult hippocampal neurogenesis. Front. Cell. Neurosci. 7, 100 (2013)
Walton NM , Shin R , Tajinda K , Heusner CL , Kogan JH , Miyake S , Chen Q , Tamura K , Matsumoto M : Adult neurogenesis transiently generates oxidative stress. PLoS One 7, e35264 (2012)
Wang Y , van der Zee M , Fodde R , Blok LJ : Wnt/β-catenin and sex hormone signaling in endometrial homeostasis and cancer. Oncotarget 1, 674–684 (2010)
Wassink TH , Piven J , Vieland VJ , Huang J , Swiderski RE , Pietila J , Braun T , Beck G , Folstein SE , Haines JL , Sheffield VC : Evidence supporting WNT2 as an autism susceptibility gene. Am. J. Med. Genet. 105, 406–413 (2001)
Watanabe S , Sato K , Hasegawa N , Kurihara T , Matsutani K , Sanada K , Hamaoka T , Fujita S , Iemitsu M : Serum C1q as a novel biomarker of sarcopenia in older adults. FASEB J. 29, 1003–1010 (2015)
Weatherbee SD , Anderson KV , Niswander LA : LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development 133, 4993–5000 (2006)
Wilkinson MB , Dias C , Magida J , Mazei-Robison M , Lobo M , Kennedy P , Dietz D , Covington H, 3rd, Russo S , Neve R , Ghose S , Tamminga C , Nestler EJ : A novel role of the WNT-dishevelled-GSK3β signaling cascade in the mouse nucleus accumbens in a social defeat model of depression. J. Neurosci. 31, 9084–9092 (2011)
Wong SY , Zhang DX , Li CC , Yip BH , Chan DC , Ling YM , Lo CS , Woo DM , Sun YY , Ma H , Mak WW , Gao T , Lee TM , Wing YK : Comparing the effects of mindfulness-based cognitive therapy and sleep psycho-education with exercise on chronic insomnia: a randomised controlled trial. Psychother. Psychosom. 86, 241–253 (2017)
Wu H , Xiong WC , Mei L : To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137, 1017–1033 (2010)
Wu J , Wang X , Chiba H , Higuchi M , Nakatani T , Ezaki O , Cui H , Yamada K , Ishimi Y : Combined intervention of soy isoflavone and moderate exercise prevents body fat elevation and bone loss in ovariectomized mice. Metabolism 53, 942–948 (2004)
Wu Y , Collier L , Qin W , Creasey G , Bauman WA , Jarvis J , Cardozo C : Electrical stimulation modulates Wnt signaling and regulates genes for the motor endplate and calcium binding in muscle of rats with spinal cord transection. BMC Neurosci. 14, 81 (2013)
Xu H , Duan J , Ning D , Li J , Liu R , Yang R , Jiang JX , Shang P : Role of Wnt signaling in fracture healing. BMB Rep. 47, 666–672 (2014)
Yamada A , Iwata T , Yamato M , Okano T , Izumi Y : Diverse functions of secreted frizzled-related proteins in the osteoblastogenesis of human multipotent mesenchymal stromal cells. Biomaterials 34, 3270–3278 (2013)
Yang Q , Du X , Fang Z , Xiong W , Li G , Liao H , Xiao J , Wang G , Li F : Effect of calcitonin gene-related peptide on the neurogenesis of rat adipose-derived stem cells in vitro. PLoS One 9, e86334 (2014)
Yang X , Arber S , William C , Li L , Tanabe Y , Jessell TM , Birchmeier C , Burden SJ : Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399–410 (2001)
Zanuso S , Sacchetti M , Sundberg CJ , Orlando G , Benvenuti P , Balducci S : Exercise in type 2 diabetes: genetic, metabolic and neuromuscular adaptations. A review of the evidence. Br. J. Sports Med. 51, 1533–1538 (2017)
Zhang B , Liang C , Bates R , Yin Y , Xiong WC , Mei L : Wnt proteins regulate acetylcholine receptor clustering in muscle cells. Mol. Brain 5, 7 (2012)
Zhang B , Luo S , Wang Q , Suzuki T , Xiong WC , Mei L : LRP4 serves as a coreceptor of agrin. Neuron 60, 285–297 (2008)
Zhang DY , Wang HJ , Tan YZ : Wnt/β-catenin signaling induces the aging of mesenchymal stem cells through the DNA damage response and the p53/p21 pathway. PLoS One 6, e21397 (2011)
Zhang J , Pan Z , Sheppard A : Both canonical and noncanonical Wnt signalling may be required for detoxification following ETP class mycotoxin exposure. Toxicol. Lett. 271, 12–19 (2017)
Zhang W , Coldefy AS , Hubbard SR , Burden SJ : Agrin binds to the N-terminal region of Lrp4 protein and stimulates association between Lrp4 and the first immunoglobulin-like domain in muscle-specific kinase (MuSK). J. Biol. Chem. 286, 40624–40630 (2011)
Zhao C , Deng W , Gage FH : Mechanisms and functional implications of adult neurogenesis. Cell 132, 645–660 (2008)
Zhong Z , Ethen NJ , Williams BO : WNT signaling in bone development and homeostasis. Wiley Interdiscip. Rev. Dev. Biol. 3, 489–500 (2014)
Zhou R , Yuan Z , Liu J : Calcitonin gene-related peptide promotes the expression of osteoblastic genes and activates the WNT signal transduction pathway in bone marrow stromal stem cells. Mol. Med. Rep. 13, 4689–4696 (2016)
Wang J , Ruan NJ , Qian L , Lei WL , Chen F , Luo ZG : Wnt/β-catenin signaling suppresses Rapsyn expression and inhibits acetylcholine receptor clustering at the neuromuscular junction. J. Biol. Chem. 283(31), 21668–21675 (2008)