65
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

PI15, a novel secreted WNT-signaling antagonist, regulates chondrocyte differentiation

, , ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 237-252 | Received 28 Dec 2023, Accepted 25 Apr 2024, Published online: 13 May 2024

References

  • Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B. The transcription factor SOX9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of SOX5 and SOX6. Genes Dev. 2002;16(21):2813–2828. doi:10.1101/gad.1017802
  • Bi W, Deng JM, Zhang Z, Behringer RR, de Crombrugghe B. SOX9 is required for cartilage formation. Nat Genet. 1999;22(1):85–89. doi:10.1038/8792
  • Baron R, Kneissel M. Wnt signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med. 2013;19(2):179–192. doi:10.1038/nm.3074
  • Kronenberg HM. Developmental regulation of the growth plate. Nature. 2003;423(6937):332–336. doi:10.1038/nature01657
  • Day TF, Guo X, Garrett-Beal L, Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell. 2005;8(5):739–750. doi:10.1016/j.devcel.2005.03.016
  • Hill TP, Später D, Taketo MM, Birchmeier W, Hartmann C. Canonical wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell. 2005;8(5):727–738. doi:10.1016/j.devcel.2005.02.013
  • Miclea RL, Karperien M, Bosch CA, van der Horst G, van der Valk MA, Kobayashi T, Kronenberg HM, Rawadi G, Akçakaya P, Löwik CW, et al. Adenomatous polyposis coli-mediated control of β-catenin is essential for both chondrogenic and osteogenic differentiation of skeletal precursors. BMC Dev Biol. 2009;9(1). doi:10.1186/1471-213X-9-26
  • Usami Y, Gunawardena AT, Francois NB, Otsuru S, Takano H, Hirose K, Matsuoka M, Suzuki A, Huang J, Qin L, et al. Possible contribution of wnt-responsive chondroprogenitors to the postnatal murine growth plate. J Bone Miner Res. 2019;34(5):964–974. doi:10.1002/jbmr.3658
  • Logan CY, Nusse R. The wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20(1):20(781–810. doi:10.1146/annurev.cellbio.20.010403.113126
  • Reinhold MI, Kapadia RM, Liao Z, Naski MC. The wnt-inducible transcription factor twist1 inhibits chondrogenesis. J Biol Chem. 2006;281(3):1381–1388. doi:10.1074/jbc.M504875200
  • Nalesso G, Sherwood J, Bertrand J, Pap T, Ramachandran M, De Bari C, Pitzalis C, Dell’accio F. Wnt-3a modulates articular chondrocyte phenotype by activating both canonical and noncanonical pathways. J Cell Biol. 2011;193(3):551–564. doi:10.1083/jcb.201011051
  • Semënov MV, Tamai K, Brott BK, Kühl M, Sokol S, He X. Head inducer Dickkopf-1 is a ligand for wnt coreceptor Lrp6. Curr Biol. 2001;11(12):951–961. doi:10.1016/S0960-9822(01)00290-1
  • Mao B, Wu W, Li Y, Hoppe D, Stannek P, Glinka A, Niehrs C. Ldl-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature. 2001;411(6835):321–325. doi:10.1038/35077108
  • Semënov M, Tamai K, He X. Sost is a ligand for LRP5/IRP6 and a wnt signaling inhibitor. J Biol Chem. 2005;280(29):26770–26775. doi:10.1074/jbc.M504308200
  • He X, Saint-Jeannet JP, Wang Y, Nathans J, Dawid I, Varmus H. A member of the frizzled protein family mediating axis induction by wnt-5a. Science. 1997;275(5306):1652–1654. doi:10.1126/science.275.5306.1652
  • Gibbs GM, Roelants K, O’Bryan MK. The cap superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins–roles in reproduction, cancer, and immune defense. Endocr Rev. 2008;29(7):865–897. doi:10.1210/er.2008-0032
  • Smith DM, Collins-Racie LA, Marigo VA, Roberts DJ, Davis NM, Hartmann C, Schweitzer R, LaVallie ER, Gamer L, McCoy J, et al. Cloning and expression of a novel cysteine-rich secreted protein family member expressed in thyroid and pancreatic mesoderm within the chicken embryo. Mech Dev. 2001;102(1–2):223–226. doi:10.1016/S0925-4773(01)00293-3
  • Nimmagadda S, Buchtová M, Fu K, Geetha-Loganathan P, Hosseini-Farahabadi S, Trachtenberg AJ, Kuo WP, Vesela I, Richman JM. Identification and functional analysis of novel facial patterning genes in the duplicated beak chicken embryo. Dev Biol. 2015;407(2):275–288. doi:10.1016/j.ydbio.2015.09.007
  • Shukunami C, Shigeno C, Atsumi T, Ishizeki K, Suzuki F, Hiraki Y. Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (pth)/pth-related peptide receptor. J Cell Biol. 1996;133(2):457–468. doi:10.1083/jcb.133.2.457
  • Haas AR, Tuan RS. Murine C3H10t1/2 multipotential cells as an in vitro model of mesenchymal chondrogenesis. Methods Mol Biol. 2000;137:383–389. doi:10.1385/1-59259-066-7:383
  • Lefebvre V, Garofalo S, Zhou G, Metsaranta M, Vuorio E, De Crombrugghe B. Characterization of primary cultures of chondrocytes from type ii collagen/beta-galactosidase transgenic mice. Matrix Biol. 1994;14(4):329–335. doi:10.1016/0945-053X(94)90199-6
  • Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-tcf signaling in colon cancer by mutations in beta-catenin or apc. Science. 1997;275(5307):1787–1790. doi:10.1126/science.275.5307.1787
  • Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT. Zebrafish prickle, a modulator of noncanonical wnt/fz signaling, regulates gastrulation movements. Curr Biol. 2003;13(8):680–685. doi:10.1016/S0960-9822(03)00240-9
  • Hariri H, Addison WN, St-Arnaud R. Ubiquitin specific peptidase usp53 regulates osteoblast versus adipocyte lineage commitment. Sci Rep. 2021;11(1):8418. doi:10.1038/s41598-021-87608-x
  • Huttlin EL, Bruckner RJ, Paulo JA, Cannon JR, Ting L, Baltier K, Colby G, Gebreab F, Gygi MP, Parzen H, et al. Architecture of the human interactome defines protein communities and disease networks. Nature. 2017;545(7655):505–509. doi:10.1038/nature22366
  • Huttlin EL, Ting L, Bruckner RJ, Gebreab F, Gygi MP, Szpyt J, Tam S, Zarraga G, Colby G, Baltier K, et al. The bioplex network: a systematic exploration of the human interactome. Cell. 2015;162(2):425–440. doi:10.1016/j.cell.2015.06.043
  • Szklarczyk D, Kirsch R, Koutrouli M, Nastou K, Mehryary F, Hachilif R, Gable AL, Fang T, Doncheva NT, Pyysalo S, et al. The string database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res. 2023;51(D1):D638–d646. doi:10.1093/nar/gkac1000
  • Denker AE, Nicoll SB, Tuan RS. Formation of cartilage-like spheroids by micromass cultures of murine c3h10t1/2 cells upon treatment with transforming growth factor-beta 1. Differentiation. 1995;59(1):25–34. doi:10.1046/j.1432-0436.1995.5910025.x
  • Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X. Ldl-receptor-related proteins in wnt signal transduction. Nature. 2000;407(6803):530–535. doi:10.1038/35035117
  • Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, Wang H, Cundy T, Glorieux FH, Lev D, et al. Ldl receptor-related protein 5 (Lrp5) affects bone accrual and eye development. Cell. 2001;107(4):513–523. doi:10.1016/S0092-8674(01)00571-2
  • Jackson A, Vayssière B, Garcia T, Newell W, Baron R, Roman-Roman S, Rawadi G. Gene array analysis of wnt-regulated genes in C3H10T1/2 cells. Bone. 2005;36(4):585–598. doi:10.1016/j.bone.2005.01.007
  • Jope RS. Lithium and gsk-3: one inhibitor, two inhibitory actions, multiple outcomes. Trends Pharmacol Sci. 2003;24(9):441–443. doi:10.1016/S0165-6147(03)00206-2
  • Hallett SA, Matsushita Y, Ono W, Sakagami N, Mizuhashi K, Tokavanich N, Nagata M, Zhou A, Hirai T, Kronenberg HM, et al. Chondrocytes in the resting zone of the growth plate are maintained in a wnt-inhibitory environment. Elife. 2021;10:10.
  • Mizuhashi K, Ono W, Matsushita Y, Sakagami N, Takahashi A, Saunders TL, Nagasawa T, Kronenberg HM, Ono N. Resting zone of the growth plate houses a unique class of skeletal stem cells. Nature. 2018;563(7730):254–258. doi:10.1038/s41586-018-0662-5
  • Abad V, Meyers JL, Weise M, Gafni RI, Barnes KM, Nilsson O, Bacher JD, Baron J. The role of the resting zone in growth plate chondrogenesis. Endocrinology. 2002;143(5):1851–1857. doi:10.1210/endo.143.5.8776
  • Newton PT, Li L, Zhou B, Schweingruber C, Hovorakova M, Xie M, Sun X, Sandhow L, Artemov AV, Ivashkin E, et al. A radical switch in clonality reveals a stem cell niche in the epiphyseal growth plate. Nature. 2019;567(7747):234–238. doi:10.1038/s41586-019-0989-6
  • Bourhis E, Tam C, Franke Y, Bazan JF, Ernst J, Hwang J, Costa M, Cochran AG, Hannoush RN. Reconstitution of a frizzled8.Wnt3a.Lrp6 signaling complex reveals multiple wnt and dkk1 binding sites on Lrp6. J Biol Chem. 2010;285(12):9172–9179. doi:10.1074/jbc.M109.092130
  • MacDonald BT, He X. Frizzled and LRP5/6 receptors for wnt/ -catenin signaling. Cold Spring Harbor Perspectives In Biology. 2012;4(12):a007880–a007880. doi:10.1101/cshperspect.a007880
  • MacDonald BT, Yokota C, Tamai K, Zeng X, He X. Wnt signal amplification via activity, cooperativity, and regulation of multiple intracellular pppsp motifs in the wnt co-receptor Lrp6. J Biol Chem. 2008;283(23):16115–16123. doi:10.1074/jbc.M800327200
  • Zeng X, Tamai K, Doble B, Li S, Huang H, Habas R, Okamura H, Woodgett J, He X. A dual-kinase mechanism for wnt co-receptor phosphorylation and activation. Nature. 2005;438(7069):873–877. doi:10.1038/nature04185
  • Tamai K, Zeng X, Liu C, Zhang X, Harada Y, Chang Z, He X. A mechanism for wnt coreceptor activation. Mol Cell. 2004;13(1):149–156. doi:10.1016/S1097-2765(03)00484-2
  • Davidson G, Wu W, Shen J, Bilic J, Fenger U, Stannek P, Glinka A, Niehrs C. Casein kinase 1 γ couples wnt receptor activation to cytoplasmic signal transduction. Nature. 2005;438(7069):867–872. doi:10.1038/nature04170
  • Chen M, Philipp M, Wang J, Premont RT, Garrison TR, Caron MG, Lefkowitz RJ, Chen W. G protein-coupled receptor kinases phosphorylate Lrp6 in the wnt pathway. J Biol Chem. 2009;284(50):35040–35048. doi:10.1074/jbc.M109.047456
  • Červenka I, Wolf J, Mašek J, Krejci P, Wilcox WR, Kozubík A, Schulte G, Gutkind JS, Bryja V. Mitogen-activated protein kinases promote wnt/beta-catenin signaling via phosphorylation of Lrp6. Mol Cell Biol. 2011;31(1):179–189. doi:10.1128/MCB.00550-10
  • Zeng X, Huang H, Tamai K, Zhang X, Harada Y, Yokota C, Almeida K, Wang J, Doble B, Woodgett J, et al. Initiation of wnt signaling: control of wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development. 2008;135(2):367–375. doi:10.1242/dev.013540
  • Kim J, Han W, Park T, Kim EJ, Bang I, Lee HS, Jeong Y, Roh K, Kim J, Kim JS, et al. Sclerostin inhibits wnt signaling through tandem interaction with two Lrp6 ectodomains. Nat Commun. 2020;11(1):5357. doi:10.1038/s41467-020-19155-4
  • Ahn VE, Chu ML, Choi HJ, Tran D, Abo A, Weis WI. Structural basis of wnt signaling inhibition by dickkopf binding to Lrp5/6. Dev Cell. 2011;21(5):862–873. doi:10.1016/j.devcel.2011.09.003
  • Kirsch N, Chang LS, Koch S, Glinka A, Dolde C, Colozza G, Benitez MDJ, De Robertis EM, Niehrs C. Angiopoietin-like 4 is a wnt signaling antagonist that promotes Lrp6 turnover. Dev Cell. 2017;43(1):71–82.e76. doi:10.1016/j.devcel.2017.09.011
  • Ding Y, Colozza G, Sosa EA, Moriyama Y, Rundle S, Salwinski L, De Robertis EM. Bighead is a wnt antagonist secreted by the xenopus spemann organizer that promotes Lrp6 endocytosis. Proc Natl Acad Sci U S A. 2018;115(39):E9135–e9144. doi:10.1073/pnas.1812117115
  • Sakane H, Yamamoto H, Kikuchi A. Lrp6 is internalized by dkk1 to suppress its phosphorylation in the lipid raft and is recycled for reuse. J Cell Sci. 2010;123(Pt 3):360–368. doi:10.1242/jcs.058008
  • Kagermeier-Schenk B, Wehner D, Ozhan-Kizil G, Yamamoto H, Li J, Kirchner K, Hoffmann C, Stern P, Kikuchi A, Schambony A, et al. Waif1/5t4 inhibits wnt/β-catenin signaling and activates noncanonical wnt pathways by modifying Lrp6 subcellular localization. Dev Cell. 2011;21(6):1129–1143. doi:10.1016/j.devcel.2011.10.015
  • Gaikwad AS, Hu J, Chapple DG, O’Bryan MK. The functions of cap superfamily proteins in mammalian fertility and disease. Hum Reprod Update. 2020;26(5):689–723. doi:10.1093/humupd/dmaa016
  • Ovcharenko I, Nobrega MA, Loots GG, Stubbs L. Ecr browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Research. 2004;32(Web Server):W280–W286. doi:10.1093/nar/gkh355
  • Lee WJ, Chatterjee S, Yap SP, Lim SL, Xing X, Kraus P, Sun W, Hu X, Sivakamasundari V, Chan HY, et al. An integrative developmental genomics and systems biology approach to identify an in vivo sox trio-mediated gene regulatory network in murine embryos. Biomed Res Int. 2017;2017(8932583):1–16. doi:10.1155/2017/8932583
  • Ohba S, He X, Hojo H, McMahon AP. Distinct transcriptional programs underlie SOX9 regulation of the mammalian chondrocyte. Cell Rep. 2015;12(2):229–243. doi:10.1016/j.celrep.2015.06.013
  • Liu CF, Lefebvre V. The transcription factors SOX9 and SOX5/SOX6 cooperate genome-wide through super-enhancers to drive chondrogenesis. Nucleic Acids Res. 2015;43(17):8183–8203. doi:10.1093/nar/gkv688
  • Hoffman LM, Garcha K, Karamboulas K, Cowan MF, Drysdale LM, Horton WA, Underhill TM. Bmp action in skeletogenesis involves attenuation of retinoid signaling. J Cell Biol. 2006;174(1):101–113. doi:10.1083/jcb.200604150
  • Weston AD, Rosen V, Chandraratna RA, Underhill TM. Regulation of skeletal progenitor differentiation by the bmp and retinoid signaling pathways. J Cell Biol. 2000;148(4):679–690. doi:10.1083/jcb.148.4.679
  • Robinson JL, Soria P, Xu M, Vrana M, Luchetti J, Lu HH, Chen J, Wadhwa S. Estrogen promotes mandibular condylar fibrocartilage chondrogenesis and inhibits degeneration via estrogen receptor alpha in female mice. Sci Rep. 2018;8(1):8527. doi:10.1038/s41598-018-26937-w
  • Yokouchi Y, Sakiyama J, Kameda T, Iba H, Suzuki A, Ueno N, Kuroiwa A. Bmp-2/-4 mediate programmed cell death in chicken limb buds. Development. 1996;122(12):3725–3734. doi:10.1242/dev.122.12.3725
  • Takemoto M, He L, Norlin J, Patrakka J, Xiao Z, Petrova T, Bondjers C, Asp J, Wallgard E, Sun Y, et al. Large-scale identification of genes implicated in kidney glomerulus development and function. Embo J. 2006;25(5):1160–1174. doi:10.1038/sj.emboj.7601014
  • Falak S, Schafer S, Baud A, Hummel O, Schulz H, Gauguier D, Hubner N, Osborne-Pellegrin M. Protease inhibitor 15, a candidate gene for abdominal aortic internal elastic lamina ruptures in the rat. Physiol Genomics. 2014;46(12):418–428. doi:10.1152/physiolgenomics.00004.2014
  • Chiquet BT, Lidral AC, Stal S, Mulliken JB, Moreno LM, Arcos-Burgos M, Valencia-Ramirez C, Blanton SH, Hecht JT. Crispld2: a novel nsclp candidate gene. Hum Mol Genet. 2007;16(18):2241–2248. doi:10.1093/hmg/ddm176
  • Koshikawa N, Nakamura T, Tsuchiya N, Isaji M, Yasumitsu H, Umeda M, Miyazaki K. Purification and identification of a novel and four known serine proteinase inhibitors secreted by human glioblastoma cells. J Biochem. 1996;119(2):334–339. doi:10.1093/oxfordjournals.jbchem.a021244
  • Prusty BK, Chowdhury SR, Gulve N, Rudel T. Peptidase inhibitor 15 (pi15) regulates chlamydial cpaf activity. Front Cell Infect Microbiol. 2018;8(183). doi:10.3389/fcimb.2018.00183
  • Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. Novel regulators of bone formation: molecular clones and activities. Science. 1988;242(4885):1528–1534. doi:10.1126/science.3201241
  • Davidson D, Blanc A, Filion D, Wang H, Plut P, Pfeffer G, Buschmann MD, Henderson JE. Fibroblast growth factor (fgf) 18 signals through fgf receptor 3 to promote chondrogenesis. J Biol Chem. 2005;280(21):20509–20515. doi:10.1074/jbc.M410148200
  • Shiang R, Thompson LM, Zhu YZ, Church DM, Fielder TJ, Bocian M, Winokur ST, Wasmuth JJ. Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell. 1994;78(2):335–342. doi:10.1016/0092-8674(94)90302-6
  • Cinque L, Forrester A, Bartolomeo R, Svelto M, Venditti R, Montefusco S, Polishchuk E, Nusco E, Rossi A, Medina DL, et al. Fgf signalling regulates bone growth through autophagy. Nature. 2015;528(7581):272–275. doi:10.1038/nature16063
  • Gill AK, McCormick PJ, Sochart D, Nalesso G. Wnt signalling in the articular cartilage: a matter of balance. Int J Experimental Path. 2023;104(2):56–63. doi:10.1111/iep.12472

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.