The Hippo signalling pathway in bone homeostasis: Under the regulation of mechanics and aging

Zhengda Li , Junqing Lin , Jing Wu , Jinlong Suo , Zuoyun Wang

Cell Proliferation ›› 2024, Vol. 57 ›› Issue (10) : e13652

PDF
Cell Proliferation ›› 2024, Vol. 57 ›› Issue (10) : e13652 DOI: 10.1002/cpr.13652
REVIEW

The Hippo signalling pathway in bone homeostasis: Under the regulation of mechanics and aging

Author information +
History +
PDF

Abstract

The Hippo signalling pathway is a conserved kinase cascade that orchestrates diverse cellular processes, such as proliferation, apoptosis, lineage commitment and stemness. With the onset of society ages, research on skeletal aging-mechanics-bone homeostasis has exploded. In recent years, aging and mechanical force in the skeletal system have gained groundbreaking research progress. Under the regulation of mechanics and aging, the Hippo signalling pathway has a crucial role in the development and homeostasis of bone. We synthesize the current knowledge on the role of the Hippo signalling pathway, particularly its downstream effectors yes-associated protein (YAP) and transcriptional co-activator with PDZ-binding motif (TAZ), in bone homeostasis. We discuss the regulation of the lineage specification and function of different skeletal cell types by the Hippo signalling pathway. The interactions of the Hippo signalling pathway with other pathways, such as Wnt, transforming growth factor beta and nuclear factor kappa-B, are also mentioned because of their importance for modulating bone homeostasis. Furthermore, YAP/TAZ have been extensively studied as mechanotransducers. Due to space limitations, we focus on reviewing how mechanical forces and aging influence cell fate, communications and homeostasis through a dysregulated Hippo signalling pathway.

Cite this article

Download citation ▾
Zhengda Li, Junqing Lin, Jing Wu, Jinlong Suo, Zuoyun Wang. The Hippo signalling pathway in bone homeostasis: Under the regulation of mechanics and aging. Cell Proliferation, 2024, 57(10): e13652 DOI:10.1002/cpr.13652

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

JinF, LiuM, ZhangD, Wang X. Translational perspective on bone-derived cytokines in inter-organ communications. Innovation. 2023;4:100365.

[2]

LvX, GaoF, CaoX. Skeletal interoception in bone homeostasis and pain. Cell Metab. 2022;34:1914-1931.

[3]

XieL, WangG, WuY, et al. Programmed surface on poly(aryl-ether-ether-ketone) initiating immune mediation and fulfilling bone regeneration sequentially. Innovation. 2021;2:100148.

[4]

LiuH, JiangD, ChiF, ZhaoB. The Hippo pathway regulates stem cell proliferation, self-renewal, and differentiation. Protein Cell. 2012;3:291-304.

[5]

AnerillasC, Mazan-Mamczarz K, HermanAB, et al. The YAP-TEAD complex promotes senescent cell survival by lowering endoplasmic reticulum stress. Nat Aging. 2023;3:1237-1250.

[6]

NavaMM, Miroshnikova YA, BiggsLC, et al. Heterochromatin-driven nuclear softening protects the genome against mechanical stress-induced damage. Cell. 2020;181:800-817.

[7]

RoelofsAJ, ZupanJ, RiemenA, et al. Joint morphogenetic cells in the adult mammalian synovium. Nat Commun. 2017;8:15040.

[8]

WangY, FangJ, LiuB, ShaoC, ShiY. Reciprocal regulation of mesenchymal stem cells and immune responses. Cell Stem Cell. 2022;29:1515-1530.

[9]

ViswanathanS, ShiY, GalipeauJ, et al. Mesenchymal stem versus stromal cells: International Society for Cell & Gene Therapy (ISCT®) Mesenchymal Stromal Cell committee position statement on nomenclature. Cytotherapy. 2019;21:1019-1024.

[10]

Zamudio-CuevasY, Plata-Rodríguez R, Fernández-TorresJ, et al. Synovial membrane mesenchymal stem cells for cartilaginous tissues repair. Mol Biol Rep. 2022;49:2503-2517.

[11]

LiP, FuL, LiaoZ, et al. Chitosan hydrogel/3D-printed poly(ϵ-caprolactone) hybrid scaffold containing synovial mesenchymal stem cells for cartilage regeneration based on tetrahedral framework nucleic acid recruitment. Biomaterials. 2021;278:121131.

[12]

TaoSC, YuanT, ZhangYL, Yin WJ, GuoSC, ZhangCQ. Exosomes derived from miR-140-5p-overexpressing human synovial mesenchymal stem cells enhance cartilage tissue regeneration and prevent osteoarthritis of the knee in a rat model. Theranostics. 2017;7:180-195.

[13]

ChanCK, SeoEY, ChenJY, et al. Identification and specification of the mouse skeletal stem cell. Cell. 2015;160:285-298.

[14]

ChanC, GulatiGS, SinhaR, et al. Identification of the human skeletal stem cell. Cell. 2018;175:43-56.

[15]

FengH, JiangB, XingW, Sun J, GreenblattMB, ZouW. Skeletal stem cells: origins, definitions, and functions in bone development and disease. Life Med. 2022;1:276-293.

[16]

JefferyEC, MannT, PoolJA, Zhao Z, MorrisonSJ. Bone marrow and periosteal skeletal stem/progenitor cells make distinct contributions to bone maintenance and repair. Cell Stem Cell. 2022;29:1547-1561.

[17]

HanY, FengH, SunJ, et al. Lkb1 deletion in periosteal mesenchymal progenitors induces osteogenic tumors through mTORC1 activation. J Clin Invest. 2019;129:1895-1909.

[18]

DebnathS, Yallowitz AR, McCormickJ, et al. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature. 2018;562:133-139.

[19]

LiuY, TianH, HuY, et al. Mechanosensitive Piezo1 is crucial for periosteal stem cell-mediated fracture healing. Int J Biol Sci. 2022;18:3961-3980.

[20]

TsukasakiM, Komatsu N, Negishi-KogaT, et al. Periosteal stem cells control growth plate stem cells during postnatal skeletal growth. Nat Commun. 2022;13:4166.

[21]

KomoriT. Regulation of proliferation, differentiation and functions of osteoblasts by Runx2. Int J Mol Sci. 2019;20:1694.

[22]

KomoriT. Whole aspect of Runx2 functions in skeletal development. Int J Mol Sci. 2022;23:5776.

[23]

ChenQ, ShouP, ZhengC, et al. Fate decision of mesenchymal stem cells: adipocytes or osteoblasts? Cell Death Differ. 2016;23:1128-1139.

[24]

ZhuS, EhnertS, RoußM, et al. From the clinical problem to the basic research-co-culture models of osteoblasts and osteoclasts. Int J Mol Sci. 2018;19:2284.

[25]

ShiY, HeG, LeeWC, McKenzie JA, SilvaMJ, LongF. Gli1 identifies osteogenic progenitors for bone formation and fracture repair. Nat Commun. 2017;8:2043.

[26]

ShenB, Tasdogan A, UbellackerJM, et al. A mechanosensitive peri-arteriolar niche for osteogenesis and lymphopoiesis. Nature. 2021;591:438-444.

[27]

Delgado-CalleJ, Bellido T. The osteocyte as a signaling cell. Physiol Rev. 2022;102:379-410.

[28]

LefebvreV, Angelozzi M, HaseebA. SOX9 in cartilage development and disease. Curr Opin Cell Biol. 2019;61:39-47.

[29]

HaseebA, KcR, AngelozziM, et al. SOX9 keeps growth plates and articular cartilage healthy by inhibiting chondrocyte dedifferentiation/osteoblastic redifferentiation. Proc Natl Acad Sci USA. 2021;118:118.

[30]

KimP, ParkJ, LeeDJ, et al. Mast4 determines the cell fate of MSCs for bone and cartilage development. Nat Commun. 2022;13:3960.

[31]

HuynhN, ZhangB, GuilakF. High-depth transcriptomic profiling reveals the temporal gene signature of human mesenchymal stem cells during chondrogenesis. FASEB J. 2019;33:358-372.

[32]

BaryawnoN, Przybylski D, KowalczykMS, et al. A cellular taxonomy of the bone marrow stroma in homeostasis and leukemia. Cell. 2019;177:1915-1932.

[33]

MizuhashiK, OnoW, MatsushitaY, et al. Resting zone of the growth plate houses a unique class of skeletal stem cells. Nature. 2018;563:254-258.

[34]

ZuscikMJ, HiltonMJ, ZhangX, Chen D, O’KeefeRJ. Regulation of chondrogenesis and chondrocyte differentiation by stress. J Clin Invest. 2008;118:429-438.

[35]

FarquharsonC, Jefferies D. Chondrocytes and longitudinal bone growth: the development of tibial dyschondroplasia. Poult Sci. 2000;79:994-1004.

[36]

ZhangP, LiX, PanC, et al. Single-cell RNA sequencing to track novel perspectives in HSC heterogeneity. Stem Cell Res Ther. 2022;13:39.

[37]

SeitaJ, Weissman IL. Hematopoietic stem cell: self-renewal versus differentiation. WIREs Syst Biol Med. 2010;2:640-653.

[38]

BoyceBF. Advances in the regulation of osteoclasts and osteoclast functions. J Dent Res. 2013;92:860-867.

[39]

YangH, WangL, ShigleyC, Yang W. Protein tyrosine phosphatases in skeletal development and diseases. Bone Res. 2022;10:10.

[40]

KongYY, Yoshida H, SarosiI, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397:315-323.

[41]

LiJ, SarosiI, YanXQ, et al. RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism. Proc Natl Acad Sci USA. 2000;97:1566-1571.

[42]

BucayN, SarosiI, DunstanCR, et al. Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998;12:1260-1268.

[43]

SimonetWS, LaceyDL, DunstanCR, et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997;89:309-319.

[44]

McDonaldMM, KhooWH, NgPY, et al. Osteoclasts recycle via osteomorphs during RANKL-stimulated bone resorption. Cell. 2021;184:1940.

[45]

GaoM, LiuX, GuoP, et al. Deciphering postnatal limb development at single-cell resolution. Iscience. 2023;26:105808.

[46]

TsukasakiM, HuynhNC, OkamotoK, et al. Stepwise cell fate decision pathways during osteoclastogenesis at single-cell resolution. Nat Metab. 2020;2:1382-1390.

[47]

HuK, ShangZ, YangX, Zhang Y, CaoL. Macrophage polarization and the regulation of bone immunity in bone homeostasis. J Inflamm Res. 2023;16:3563-3580.

[48]

ChenS, NiS, LiuC, et al. Neglected immunoregulation: M2 polarization of macrophages triggered by low-dose irradiation plays an important role in bone regeneration. J Cell Mol Med. 2023;27:1095-1109.

[49]

ZhaL, HeL, LiangY, et al. TNF-α contributes to postmenopausal osteoporosis by synergistically promoting RANKL-induced osteoclast formation. Biomed Pharmacother. 2018;102:369-374.

[50]

BartokB, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010;233:233-255.

[51]

CulemannS, Grüneboom A, Nicolás-Ávila , et al. Locally renewing resident synovial macrophages provide a protective barrier for the joint. Nature. 2019;572:670-675.

[52]

FahyN, de Vries-van MM, LehmannJ, et al. Human osteoarthritic synovium impacts chondrogenic differentiation of mesenchymal stem cells via macrophage polarisation state. Osteoarthr Cartil. 2014;22:1167-1175.

[53]

ZhangH, LinC, ZengC, et al. Synovial macrophage M1 polarisation exacerbates experimental osteoarthritis partially through R-spondin-2. Ann Rheum Dis. 2018;77:1524-1534.

[54]

NygaardG, Firestein GS. Restoring synovial homeostasis in rheumatoid arthritis by targeting fibroblast-like synoviocytes. Nat Rev Rheumatol. 2020;16:316-333.

[55]

WuZ, MaD, YangH, et al. Fibroblast-like synoviocytes in rheumatoid arthritis: surface markers and phenotypes. Int Immunopharmacol. 2021;93:107392.

[56]

HanD, FangY, TanX, et al. The emerging role of fibroblast-like synoviocytes-mediated synovitis in osteoarthritis: an update. J Cell Mol Med. 2020;24:9518-9532.

[57]

BaoC, ZhuS, SongK, He C. HK2: a potential regulator of osteoarthritis via glycolytic and non-glycolytic pathways. Cell Commun Signal. 2022;20:132.

[58]

CaoX, WuS, WangX, Huang J, ZhangW, LiangC. Receptor tyrosine kinase C-kit promotes a destructive phenotype of FLS in osteoarthritis via intracellular EMT signaling. Mol Med. 2023;29:38.

[59]

ChenX, GongW, ShaoX, et al. METTL3-mediated m(6)A modification of ATG7 regulates autophagy-GATA4 axis to promote cellular senescence and osteoarthritis progression. Ann Rheum Dis. 2022;81:87-99.

[60]

EndishaH, DattaP, SharmaA, et al. MicroRNA-34a-5p promotes joint destruction during osteoarthritis. Arthritis Rheumatol. 2021;73:426-439.

[61]

MayorR, Theveneau E. The neural crest. Development. 2013;140:2247-2251.

[62]

SoldatovR, KauckaM, KastritiME, et al. Spatiotemporal structure of cell fate decisions in murine neural crest. Science. 2019;364:eaas9536.

[63]

Le DouarinNM, Creuzet S, CoulyG, DupinE. Neural crest cell plasticity and its limits. Development. 2004;131:4637-4650.

[64]

LiaoJ, HuangY, WangQ, et al. Gene regulatory network from cranial neural crest cells to osteoblast differentiation and calvarial bone development. Cell Mol Life Sci. 2022;79:158.

[65]

KamalakarA, McKinney JM, SalinasDD, et al. JAGGED1 stimulates cranial neural crest cell osteoblast commitment pathways and bone regeneration independent of canonical NOTCH signaling. Bone. 2021;143:115657.

[66]

Simões-CostaM, Bronner ME. Establishing neural crest identity: a gene regulatory recipe. Development. 2015;142:242-257.

[67]

RochaM, SinghN, AhsanK, Beiriger A, PrinceVE. Neural crest development: insights from the zebrafish. Dev Dyn. 2020;249:88-111.

[68]

Mori-AkiyamaY, Akiyama H, RowitchDH, de CrombruggheB. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc Natl Acad Sci USA. 2003;100:9360-9365.

[69]

FuM, HuY, LanT, GuanKL, LuoT, LuoM. The Hippo signalling pathway and its implications in human health and diseases. Signal Transduct Tar. 2022;7:376.

[70]

XuT, WangW, ZhangS, Stewart RA, YuW. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development. 1995;121:1053-1063.

[71]

CunninghamR, HansenCG. The Hippo pathway in cancer: YAP/TAZ and TEAD as therapeutic targets in cancer. Clin Sci. 2022;136:197-222.

[72]

RussellJO, Camargo FD. Hippo signalling in the liver: role in development, regeneration and disease. Nat Rev Gastroenterol Hepatol. 2022;19:297-312.

[73]

WuS, LiuY, ZhengY, Dong J, PanD. The TEAD/TEF family protein scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell. 2008;14:388-398.

[74]

LorthongpanichC, Thumanu K, TangkiettrakulK, et al. YAP as a key regulator of adipo-osteogenic differentiation in human MSCs. Stem Cell Res Ther. 2019;10:402.

[75]

PanJX, XiongL, ZhaoK, et al. YAP promotes osteogenesis and suppresses adipogenic differentiation by regulating β-catenin signaling. Bone Res. 2018;6:18.

[76]

HongJH, HwangES, McManusMT, et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science. 2005;309:1074-1078.

[77]

TangY, RoweRG, BotvinickEL, et al. MT1-MMP-dependent control of skeletal stem cell commitment via a β1-integrin/YAP/TAZ signaling axis. Dev Cell. 2013;25:402-416.

[78]

LiJ, YanJF, WanQQ, et al. Matrix stiffening by self-mineralizable guided bone regeneration. Acta Biomater. 2021;125:112-125.

[79]

SeoE, Basu-Roy U, GunaratnePH, et al. SOX2 regulates YAP1 to maintain stemness and determine cell fate in the osteo-adipo lineage. Cell Rep. 2013;3:2075-2087.

[80]

KegelmanCD, Nijsure MP, MoharrerY, et al. YAP and TAZ promote periosteal osteoblast precursor expansion and differentiation for fracture repair. J Bone Miner Res. 2021;36:143-157.

[81]

XiongJ, Almeida M, O’BrienCA. The YAP/TAZ transcriptional co-activators have opposing effects at different stages of osteoblast differentiation. Bone. 2018;112:1-9.

[82]

SuoJ, FengX, LiJ, et al. VGLL4 promotes osteoblast differentiation by antagonizing TEADs-inhibited Runx2 transcription. Sci Adv. 2020;6:6.

[83]

KegelmanCD, Coulombe JC, JordanKM, et al. YAP and TAZ mediate osteocyte perilacunar/canalicular remodeling. J Bone Miner Res. 2020;35:196-210.

[84]

LiW, DengY, FengB, Mak KKL. Mst1/2 kinases modulate glucose uptake for osteoblast differentiation and bone formation. J Bone Miner Res. 2018;33:1183-1195.

[85]

ZhangQ, WuB, YuanY, et al. CGRP-modulated M2 macrophages regulate osteogenesis of MC3T3-E1 via Yap1. Arch Biochem Biophys. 2021;697:108697.

[86]

LiY, YangS, QinL, YangS. TAZ is required for chondrogenesis and skeletal development. Cell Discov. 2021;7:26.

[87]

DengY, WuA, LiP, et al. Yap1 regulates multiple steps of chondrocyte differentiation during skeletal development and bone repair. Cell Rep. 2016;14:2224-2237.

[88]

GotoH, NishioM, ToY, et al. Loss of Mob1a/b in mice results in chondrodysplasia due to YAP1/TAZ-TEAD-dependent repression of SOX9. Development. 2018;145:dev159244.

[89]

VanyaiHK, PrinF, GuillerminO, et al. Control of skeletal morphogenesis by the Hippo-YAP/TAZ pathway. Development. 2020;147:dev187187.

[90]

LiM, NingJ, WangJ, Yan Q, ZhaoK, JiaX. SETD7 regulates chondrocyte differentiation and glycolysis via the Hippo signaling pathway and HIF-1α. Int J Mol Med. 2021;48:210.

[91]

LundinV, SugdenWW, TheodoreLN, et al. YAP regulates hematopoietic stem cell formation in response to the biomechanical forces of blood flow. Dev Cell. 2020;52:446-460.

[92]

AlthoffMJ, NayakRC, HegdeS, et al. Yap1-Scribble polarization is required for hematopoietic stem cell division and fate. Blood. 2020;136:1824-1836.

[93]

LeeDH, KimTS, LeeD, LimDS. Mammalian sterile 20 kinase 1 and 2 are important regulators of hematopoietic stem cells in stress condition. Sci Rep. 2018;8:942.

[94]

LeeJ, YounBU, KimK, et al. Mst2 controls bone homeostasis by regulating osteoclast and osteoblast differentiation. J Bone Miner Res. 2015;30:1597-1607.

[95]

YangW, LuX, ZhangT, et al. TAZ inhibits osteoclastogenesis by attenuating TAK1/NF-κB signaling. Bone Res. 2021;9:33.

[96]

LiH, HuS, WuR, et al. 11β-hydroxysteroid dehydrogenase type 1 facilitates osteoporosis by turning on osteoclastogenesis through Hippo signaling. Int J Biol Sci. 2023;19:3628-3639.

[97]

ZhaoL, GuanH, SongC, et al. YAP1 is essential for osteoclastogenesis through a TEADs-dependent mechanism. Bone. 2018;110:177-186.

[98]

LiQ, HanG, LiuD, ZhouY. Force-induced decline of TEA domain family member 1 contributes to osteoclastogenesis via regulation of osteoprotegerin. Arch Oral Biol. 2019;100:23-32.

[99]

FengY, LiangY, ZhuX, et al. The signaling protein Wnt5a promotes TGFβ1-mediated macrophage polarization and kidney fibrosis by inducing the transcriptional regulators Yap/Taz. J Biol Chem. 2018;293:19290-19302.

[100]

LiC, JinY, WeiS, et al. Hippo signaling controls NLR family pyrin domain containing 3 activation and governs immunoregulation of mesenchymal stem cells in mouse liver injury. Hepatology. 2019;70:1714-1731.

[101]

ZhouX, LiW, WangS, et al. YAP aggravates inflammatory bowel disease by regulating M1/M2 macrophage polarization and gut microbial homeostasis. Cell Rep. 2019;27:1176-1189.

[102]

MeliVS, AtchaH, VeerasubramanianPK, et al. YAP-mediated mechanotransduction tunes the macrophage inflammatory response. Sci Adv. 2020;6:eabb8471.

[103]

YangJ, LiS, LiZ, et al. Targeting YAP1-regulated glycolysis in fibroblast-like synoviocytes impairs macrophage infiltration to ameliorate diabetic osteoarthritis progression. Adv Sci. 2024;11:e2304617.

[104]

BottiniA, WuDJ, AiR, et al. PTPN14 phosphatase and YAP promote TGFβ signalling in rheumatoid synoviocytes. Ann Rheum Dis. 2019;78:600-609.

[105]

SymonsRA, Colella F, CollinsFL, et al. Targeting the IL-6-Yap-Snail signalling axis in synovial fibroblasts ameliorates inflammatory arthritis. Ann Rheum Dis. 2022;81:214-224.

[106]

ZhouW, ShenQ, WangH, et al. Knockdown of YAP/TAZ inhibits the migration and invasion of fibroblast synovial cells in rheumatoid arthritis by regulating autophagy. J Immunol Res. 2020;2020:9510594.

[107]

DuY, CuiR, TianN, Chen M, ZhangX-L, DaiS-M. Regulation of type I interferon signature by VGLL3 in the fibroblast-like synoviocytes of rheumatoid arthritis patients via targeting the Hippo pathway. Arthritis Res Ther. 2022;24:188.

[108]

CollinsFL, Roelofs AJ, SymonsRA, et al. Taxonomy of fibroblasts and progenitors in the synovial joint at single-cell resolution. Ann Rheum Dis. 2023;82:428-437.

[109]

HindleyCJ, Condurat AL, MenonV, et al. The Hippo pathway member YAP enhances human neural crest cell fate and migration. Sci Rep. 2016;6:23208.

[110]

WangJ, XiaoY, HsuCW, et al. Yap and Taz play a crucial role in neural crest-derived craniofacial development. Development. 2016;143:504-515.

[111]

SunZ, DaFC, MorenoM, et al. FoxO6 regulates Hippo signaling and growth of the craniofacial complex. PLoS Genet. 2018;14:e1007675.

[112]

ZhaoX, TangL, LeTP, et al. Yap and Taz promote osteogenesis and prevent chondrogenesis in neural crest cells in vitro and in vivo. Sci Signal. 2022;15:eabn9009.

[113]

LiuK, NiJD, LiWZ, et al. The Sp1/FOXC1/HOTTIP/LATS2/YAP/β-catenin cascade promotes malignant and metastatic progression of osteosarcoma. Mol Oncol. 2020;14:2678-2695.

[114]

LiY, YangS, YangS. Rb1 negatively regulates bone formation and remodeling through inhibiting transcriptional regulation of YAP in Glut1 and OPG expression and glucose metabolism in male mice. Mol Metab. 2022;66:101630.

[115]

LarssonJ, OhishiM, GarrisonB, et al. Nf2/merlin regulates hematopoietic stem cell behavior by altering microenvironmental architecture. Cell Stem Cell. 2008;3:221-227.

[116]

MartínezTI, Steimle JD, ZhaoX, WangJ, MartinJF. LATS1/2 control TGFB-directed epithelial-to-mesenchymal transition in the murine dorsal cranial neuroepithelium through YAP regulation. Development. 2022;149:dev200860.

[117]

GoodwinAF, ChenCP, VoNT, BushJO, KleinOD. YAP/TAZ regulate elevation and bone formation of the mouse secondary palate. J Dent Res. 2020;99:1387-1396.

[118]

ManderfieldLJ, Engleka KA, AghajanianH, et al. Pax3 and hippo signaling coordinate melanocyte gene expression in neural crest. Cell Rep. 2014;9:1885-1895.

[119]

ZhangX, CaiD, ZhouF, et al. Targeting downstream subcellular YAP activity as a function of matrix stiffness with Verteporfin-encapsulated chitosan microsphere attenuates osteoarthritis. Biomaterials. 2020;232:119724.

[120]

DengY, LuJ, LiW, et al. Reciprocal inhibition of YAP/TAZ and NF-κB regulates osteoarthritic cartilage degradation. Nat Commun. 2018;9:4564.

[121]

CleversH, NusseR. Wnt/β-catenin signaling and disease. Cell. 2012;149:1192-1205.

[122]

BaronR, Kneissel M. WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med. 2013;19:179-192.

[123]

AkoumianakisI, Polkinghorne M, AntoniadesC. Non-canonical WNT signalling in cardiovascular disease: mechanisms and therapeutic implications. Nat Rev Cardiol. 2022;19:783-797.

[124]

ZhouT, GaoB, FanY, et al. Piezo1/2 mediate mechanotransduction essential for bone formation through concerted activation of NFAT-YAP1-ß-catenin. Elife. 2020;9:9.

[125]

AzzolinL, Zanconato F, BresolinS, et al. Role of TAZ as mediator of Wnt signaling. Cell. 2012;151:1443-1456.

[126]

JiaoS, LiC, HaoQ, et al. VGLL4 targets a TCF4-TEAD4 complex to coregulate Wnt and Hippo signalling in colorectal cancer. Nat Commun. 2017;8:14058.

[127]

WangM, ZhaoX, QiuR, et al. Lymph node metastasis-derived gastric cancer cells educate bone marrow-derived mesenchymal stem cells via YAP signaling activation by exosomal Wnt5a. Oncogene. 2021;40:2296-2308.

[128]

WangP, HuangL, YangF, Chen W, BaiD, GuoY. YAP/TEAD1 and β-catenin/LEF1 synergistically induce estrogen receptor α to promote osteogenic differentiation of bone marrow stromal cells. Medcomm. 2023;4:e246.

[129]

ByunMR, HwangJH, KimAR, et al. Canonical Wnt signalling activates TAZ through PP1A during osteogenic differentiation. Cell Death Differ. 2014;21:854-863.

[130]

Haffner-LuntzerM, Ragipoglu D, AhmadM, et al. Wnt1 boosts fracture healing by enhancing bone formation in the fracture callus. J Bone Miner Res. 2023;38:749-764.

[131]

YangB, SunH, SongF, Yu M, WuY, WangJ. YAP1 negatively regulates chondrocyte differentiation partly by activating the β-catenin signaling pathway. Int J Biochem Cell Biol. 2017;87:104-113.

[132]

ZhangY, ZuoT, McVicarA, Yang HL, LiYP, ChenW. Runx1 is a key regulator of articular cartilage homeostasis by orchestrating YAP, TGFβ and Wnt signaling in articular cartilage formation and osteoarthritis. Bone Res. 2022;10:63.

[133]

KumarD, NitzanE, KalcheimC. YAP promotes neural crest emigration through interactions with BMP and Wnt activities. Cell Commun Signal. 2019;17:69.

[134]

ChenG, DengC, LiYP. TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci. 2012;8:272-288.

[135]

HosokawaR, UrataM, HanJ, et al. TGF-beta mediated Msx2 expression controls occipital somites-derived caudal region of skull development. Dev Biol. 2007;310:140-153.

[136]

QiuT, WuX, ZhangF, Clemens TL, WanM, CaoX. TGF-beta type II receptor phosphorylates PTH receptor to integrate bone remodelling signalling. Nat Cell Biol. 2010;12:224-234.

[137]

LuoK. Signaling cross talk between TGF-β/Smad and other signaling pathways. Cold Spring Harb Perspect Biol. 2017;9(1):a022137.

[138]

WeiQ, HolleA, LiJ, et al. BMP-2 signaling and mechanotransduction synergize to drive osteogenic differentiation via YAP/TAZ. Adv Sci. 2020;7:1902931.

[139]

YinX, Choudhury M, KangJH, et al. Hexokinase 2 couples glycolysis with the profibrotic actions of TGF-β. Sci Signal. 2019;12:eaax4067.

[140]

de AraújoFV, Carrillo-Gálvez AB, MartínF, AndersonP. TGF-β and mesenchymal stromal cells in regenerative medicine, autoimmunity and cancer. Cytokine Growth Factor Rev. 2018;43:25-37.

[141]

ReichenbachM, MendezPL, DaSMC, et al. Differential impact of fluid shear stress and YAP/TAZ on BMP/TGF-β induced osteogenic target genes. Adv Biol. 2021;5:e2000051.

[142]

YangB, SunH, XuX, ZhongH, WuY, WangJ. YAP1 inhibits the induction of TNF-α-stimulated bone-resorbing mediators by suppressing the NF-κB signaling pathway in MC3T3-E1 cells. J Cell Physiol. 2020;235:4698-4708.

[143]

WangL, YouX, LotinunS, Zhang L, WuN, ZouW. Mechanical sensing protein PIEZO1 regulates bone homeostasis via osteoblast-osteoclast crosstalk. Nat Commun. 2020;11:282.

[144]

DingB, XiaoL, XuH. YAP1 controls degeneration of human cartilage chondrocytes in response to mechanical tension. Cell Biol Int. 2022;46:1637-1648.

[145]

YuH, WangH, LiuJ, HuangT, ManY, XiangL. The effect of ROS-YAP crosstalk on osteoimmune response orchestrating osteogenesis. Cell Cycle. 2023;22:1391-1405.

[146]

DupontS, MorsutL, AragonaM, et al. Role of YAP/TAZ in mechanotransduction. Nature. 2011;474:179-183.

[147]

AragonaM, Panciera T, ManfrinA, et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell. 2013;154:1047-1059.

[148]

WangL, YouX, ZhangL, Zhang C, ZouW. Mechanical regulation of bone remodeling. Bone Res. 2022;10:16.

[149]

ShiH, ZhouK, WangM, et al. Integrating physicomechanical and biological strategies for BTE: biomaterials-induced osteogenic differentiation of MSCs. Theranostics. 2023;13:3245-3275.

[150]

KimJ, JoH, HongH, et al. Actin remodelling factors control ciliogenesis by regulating YAP/TAZ activity and vesicle trafficking. Nat Commun. 2015;6:6781.

[151]

HalderG, DupontS, PiccoloS. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat Rev Mol Cell Biol. 2012;13:591-600.

[152]

YinF, YuJ, ZhengY, Chen Q, ZhangN, PanD. Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell. 2013;154:1342-1355.

[153]

LiW, ZhaoJ, WangJ, et al. ROCK-TAZ signaling axis regulates mechanical tension-induced osteogenic differentiation of rat cranial sagittal suture mesenchymal stem cells. J Cell Physiol. 2020;235:5972-5984.

[154]

StanleyA, HeoSJ, MauckRL, Mourkioti F, ShoreEM. Elevated BMP and mechanical signaling through YAP1/RhoA poises FOP mesenchymal progenitors for osteogenesis. J Bone Miner Res. 2019;34:1894-1909.

[155]

ElbediwyA, Vincent-Mistiaen ZI, Spencer-DeneB, et al. Integrin signalling regulates YAP and TAZ to control skin homeostasis. Development. 2016;143:1674-1687.

[156]

WangS, Englund E, KjellmanP, et al. CCM3 is a gatekeeper in focal adhesions regulating mechanotransduction and YAP/TAZ signalling. Nat Cell Biol. 2021;23:758-770.

[157]

ChangL, Azzolin L, Di BiagioD, et al. The SWI/SNF complex is a mechanoregulated inhibitor of YAP and TAZ. Nature. 2018;563:265-269.

[158]

TakeichiM. The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci. 2007;8:11-20.

[159]

BertocchiC, WangY, RavasioA, et al. Nanoscale architecture of cadherin-based cell adhesions. Nat Cell Biol. 2017;19:28-37.

[160]

Benham-PyleBW, PruittBL, NelsonWJ. Cell adhesion. Mechanical strain induces E-cadherin-dependent Yap1 and β-catenin activation to drive cell cycle entry. Science. 2015;348:1024-1027.

[161]

GiampietroC, Disanza A, BraviL, et al. The actin-binding protein EPS8 binds VE-cadherin and modulates YAP localization and signaling. J Cell Biol. 2015;211:1177-1192.

[162]

WuJ, Minikes AM, GaoM, et al. Intercellular interaction dictates cancer cell ferroptosis via NF2-YAP signalling. Nature. 2019;572:402-406.

[163]

KeW, LiaoZ, LiangH, et al. Stiff substrate induces nucleus pulposus cell ferroptosis via YAP and N-cadherin mediated mechanotransduction. Adv Healthc Mater. 2023;12:e2300458.

[164]

ZhangZ, ShaB, ZhaoL, et al. Programmable integrin and N-cadherin adhesive interactions modulate mechanosensing of mesenchymal stem cells by cofilin phosphorylation. Nat Commun. 2022;13:6854.

[165]

ZhangC, ZhuH, RenX, et al. Mechanics-driven nuclear localization of YAP can be reversed by N-cadherin ligation in mesenchymal stem cells. Nat Commun. 2021;12:6229.

[166]

YuFX, ZhaoB, PanupinthuN, et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell. 2012;150:780-791.

[167]

KhalafallaFG, GreeneS, KhanH, et al. P2Y(2) nucleotide receptor prompts human cardiac progenitor cell activation by modulating Hippo signaling. Circ Res. 2017;121:1224-1236.

[168]

MederosYSM, StorchU, MeibersS, et al. Gq-coupled receptors as mechanosensors mediating myogenic vasoconstriction. EMBO J. 2008;27:3092-3103.

[169]

GaoJ, HeL, ZhouL, et al. Mechanical force regulation of YAP by F-actin and GPCR revealed by super-resolution imaging. Nanoscale. 2020;12:2703-2714.

[170]

CaiH, XuY. The role of LPA and YAP signaling in long-term migration of human ovarian cancer cells. Cell Commun Signal. 2013;11:31.

[171]

YuFX, ZhangY, ParkHW, et al. Protein kinase A activates the Hippo pathway to modulate cell proliferation and differentiation. Genes Dev. 2013;27:1223-1232.

[172]

ZhongG, SuS, LiJ, et al. Activation of Piezo1 promotes osteogenic differentiation of aortic valve interstitial cell through YAP-dependent glutaminolysis. Sci Adv. 2023;9:eadg478.

[173]

YingK, LiuH, TarkhovAE, et al. Causality-enriched epigenetic age uncouples damage and adaptation. Nat Aging. 2024;4:231-246.

[174]

BaoH, CaoJ, ChenM, et al. Biomarkers of aging. Sci China Life Sci. 2023;66:893-1066.

[175]

Sladitschek-MartensHL, Guarnieri A, BrumanaG, et al. YAP/TAZ activity in stromal cells prevents ageing by controlling cGAS-STING. Nature. 2022;607:790-798.

[176]

XuX, ShenX, WangJ, et al. YAP prevents premature senescence of astrocytes and cognitive decline of Alzheimer’s disease through regulating CDK6 signaling. Aging Cell. 2021;20:e13465.

[177]

YueX, CuiJ, SunZ, et al. Nuclear softening mediated by Sun2 suppression delays mechanical stress-induced cellular senescence. Cell Death Dis. 2023;9:167.

[178]

DuK, Maeso-Díaz R, OhSH, et al. Targeting YAP-mediated HSC death susceptibility and senescence for treatment of liver fibrosis. Hepatology. 2023;77:1998-2015.

[179]

YuB, HuoL, LiuY, et al. PGC-1α controls skeletal stem Cell fate and bone-fat balance in osteoporosis and skeletal aging by inducing TAZ. Cell Stem Cell. 2018;23:193-209.

[180]

SantinonG, BrianI, PocaterraA, et al. dNTP metabolism links mechanical cues and YAP/TAZ to cell growth and oncogene-induced senescence. EMBO J. 2018;37:e97780.

[181]

RenX, HuB, SongM, et al. Maintenance of nucleolar homeostasis by CBX4 alleviates senescence and osteoarthritis. Cell Rep. 2019;26:3643-3656.

[182]

ChenF, HouW, YuX, et al. CBX4 deletion promotes tumorigenesis under Kras(G12D) background by inducing genomic instability. Signal Transduct Target Ther. 2023;8:343.

[183]

LiCJ, XiaoY, YangM, et al. Long noncoding RNA Bmncr regulates mesenchymal stem cell fate during skeletal aging. J Clin Invest. 2018;128:5251-5266.

[184]

ZhangL, ZhangC, ZhengJ, et al. miR-155-5p/Bmal1 modulates the senescence and osteogenic differentiation of mouse BMSCs through the Hippo signaling pathway. Stem Cell Rev Rep. 2024;20:554-567.

[185]

DriskillJH, PanD. Control of stem cell renewal and fate by YAP and TAZ. Nat Rev Mol Cell Biol. 2023;24:895-911.

RIGHTS & PERMISSIONS

2024 The Authors. Cell Proliferation published by Beijing Institute for Stem Cell and Regenerative Medicine and John Wiley & Sons Ltd.

AI Summary AI Mindmap
PDF

149

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/