Role of Agrin in tissue repair and regeneration: From mechanisms to therapeutic opportunities (Review)
- Authors:
- Xiang Li
- Yuan Xu
- Jing-Xing Si
- Fang Gu
- Ying-Yu Ma
-
Affiliations: Center for Plastic and Reconstructive Surgery, Department of Plastic and Reconstructive Surgery, Zhejiang Provincial People's Hospital (Affiliated People's Hospital), Hangzhou Medical College, Hangzhou, Zhejiang 310014, P.R. China, Department of Gastrointestinal Surgery, Ningbo Medical Center Lihuili Hospital, Ningbo, Zhejiang 315048, P.R. China, Department of Paediatrics, Zhejiang Provincial People's Hospital, Affiliated People's Hospital, Hangzhou Medical College, Hangzhou, Zhejiang 310014, P.R. China - Published online on: September 11, 2024 https://doi.org/10.3892/ijmm.2024.5422
- Article Number: 98
-
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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 |
 |
|
Mao AS and Mooney DJ: Regenerative medicine: Current therapies and future directions. Proc Natl Acad Sci USA. 112:14452–14459. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Tsim KW, Ruegg MA, Escher G, Kroger S and McMahan UJ: cDNA that encodes active agrin. Neuron. 8:677–689. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Chakraborty S and Hong W: Linking extracellular matrix agrin to the hippo pathway in liver cancer and beyond. Cancers (Basel). 10:452018. View Article : Google Scholar : PubMed/NCBI | |
|
Xie T, Xu G, Liu Y, Quade B, Lin W and Bai XC: Structural insights into the assembly of the agrin/LRP4/MuSK signaling complex. Proc Natl Acad Sci USA. 120:e23004531202023. View Article : Google Scholar : PubMed/NCBI | |
|
Adamiok-Ostrowska A, Grzanka M and Czarnocka B: Agrin is a novel oncogenic protein in thyroid cancer. Oncol Lett. 26:4832023. View Article : Google Scholar : PubMed/NCBI | |
|
Han L, Shi H, Ma S, Luo Y, Sun W, Li S, Zhang N, Jiang X, Gao Y, Huang Z, et al: Agrin promotes non-small cell lung cancer progression and stimulates regulatory T cells via increasing IL-6 secretion through PI3K/AKT pathway. Front Oncol. 11:8044182022. View Article : Google Scholar : PubMed/NCBI | |
|
Wang ZQ, Sun XL, Wang YL and Miao YL: Agrin promotes the proliferation, invasion and migration of rectal cancer cells via the WNT signaling pathway to contribute to rectal cancer progression. J Recept Signal Transduct Res. 41:363–370. 2021. View Article : Google Scholar | |
|
Sarig R, Rimmer R, Bassat E, Zhang L, Umansky KB, Lendengolts D, Perlmoter G, Yaniv K and Tzahor E: Transient p53-mediated regenerative senescence in the injured heart. Circulation. 139:2491–2494. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Bassat E, Mutlak YE, Genzelinakh A, Shadrin IY, Baruch Umansky K, Yifa O, Kain D, Rajchman D, Leach J, Riabov Bassat D, et al: The extracellular matrix protein agrin promotes heart regeneration in mice. Nature. 547:179–184. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li L, Xiong WC and Mei L: Neuromuscular junction formation, aging, and disorders. Annu Rev Physiol. 80:159–188. 2018. View Article : Google Scholar | |
|
Oentaryo MJ, Tse AC and Lee CW: Neuronal MT1-MMP mediates ECM clearance and Lrp4 cleavage for agrin deposition and signaling in presynaptic development. J Cell Sci. 133:jcs2467102020. View Article : Google Scholar : PubMed/NCBI | |
|
Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP and Sanes JR: Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell. 85:525–535. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Burgess RW, Nguyen QT, Son YJ, Lichtman JW and Sanes JR: Alternatively spliced isoforms of nerve- and muscle-derived agrin: Their roles at the neuromuscular junction. Neuron. 23:33–44. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Lin W, Dominguez B, Yang J, Aryal P, Brandon EP, Gage FH and Lee KF: Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism. Neuron. 46:569–579. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Misgeld T, Kummer TT, Lichtman JW and Sanes JR: Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter. Proc Natl Acad Sci USA. 102:11088–11093. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Kim N and Burden SJ: MuSK controls where motor axons grow and form synapses. Nat Neurosci. 11:19–27. 2008. View Article : Google Scholar | |
|
Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR and Lee KF: Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature. 410:1057–1064. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, Birchmeier C and Burden SJ: Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron. 30:399–410. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Grabrucker S, Marizzoni M, Silajdzic E, Lopizzo N, Mombelli E, Nicolas S, Dohm-Hansen S, Scassellati C, Moretti DV, Rosa M, et al: Microbiota from Alzheimer's patients induce deficits in cognition and hippocampal neurogenesis. Brain. 146:4916–4934. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Goncalves JT, Schafer ST and Gage FH: Adult neurogenesis in the hippocampus: From stem cells to behavior. Cell. 167:897–914. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ming GL and Song H: Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron. 70:687–702. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang H, Sathyamurthy A, Liu F, Li L, Zhang L, Dong Z, Cui W, Sun X, Zhao K, Wang H, et al: Agrin-Lrp4-Ror2 signaling regulates adult hippocampal neurogenesis in mice. Elife. 8:e453032019. View Article : Google Scholar : PubMed/NCBI | |
|
Yang JF, Cao G, Koirala S, Reddy LV and Ko CP: Schwann cells express active agrin and enhance aggregation of acetylcholine receptors on muscle fibers. J Neurosci. 21:9572–9584. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Yu J, Oentaryo MJ and Lee CW: Local protein synthesis of neuronal MT1-MMP for agrin-induced presynaptic development. Development. 148:dev1990002021. View Article : Google Scholar : PubMed/NCBI | |
|
Uyen Dao TM, Barbeau S, Messeant J, Della-Gaspera B, Bouceba T, Semprez F, Legay C and Dobbertin A: The collagen ColQ binds to LRP4 and regulates the activation of the Muscle-Specific Kinase-LRP4 receptor complex by agrin at the neuromuscular junction. J Biol Chem. 299:1049622023. View Article : Google Scholar : PubMed/NCBI | |
|
Gao H, Zhao Z, Li J, Guo Z, Zhang F, Wang K, Bai X, Wang Q, Guan Y, Wang Y, et al: Platelet-rich plasma promotes skeletal muscle regeneration and neuromuscular functional reconstitution in a concentration-dependent manner in a rat laceration model. Biochem Biophys Res Commun. 672:185–192. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Feng Z and Ko CP: Schwann cells promote synaptogenesis at the neuromuscular junction via transforming growth factor-beta1. J Neurosci. 28:9599–9609. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang BG, Quigley AF, Bourke JL, Nowell CJ, Myers DE, Choong PF and Kapsa RM: Combination of agrin and laminin increase acetylcholine receptor clustering and enhance functional neuromuscular junction formation In vitro. Dev Neurobiol. 76:551–565. 2016. View Article : Google Scholar | |
|
Ma L, Pan L, Liu W, Liu Y, Xiang X, Pan Y, Zhang X and Jin L: Agrin influences botulinum neurotoxin a-induced nerve sprouting via miR-144-agrin-MuSK signaling. Front Cell Dev Biol. 8:152020. View Article : Google Scholar : PubMed/NCBI | |
|
Gilhus NE, Tzartos S, Evoli A, Palace J, Burns TM and Verschuuren JJGM: Myasthenia gravis. Nat Rev Dis Primers. 5:302019. View Article : Google Scholar : PubMed/NCBI | |
|
Lazaridis K and Tzartos SJ: Autoantibody specificities in myasthenia gravis; implications for improved diagnostics and therapeutics. Front Immunol. 11:2122020. View Article : Google Scholar : PubMed/NCBI | |
|
Yan M, Xing GL, Xiong WC and Mei L: Agrin and LRP4 antibodies as new biomarkers of myasthenia gravis. Ann N Y Acad Sci. 1413:126–135. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Yu Z, Zhang M, Jing H, Chen P, Cao R, Pan J, Luo B, Yu Y, Quarles BM, Xiong W, et al: Characterization of LRP4/agrin antibodies from a patient with myasthenia gravis. Neurology. 97:e975–e987. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Rivner MH, Quarles BM, Pan JX, Yu Z, Howard JF Jr, Corse A, Dimachkie MM, Jackson C, Vu T, Small G, et al: Clinical features of LRP4/agrin-antibody-positive myasthenia gravis: A multicenter study. Muscle Nerve. 62:333–343. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Ohno K, Ohkawara B and Ito M: Agrin-LRP4-MuSK signaling as a therapeutic target for myasthenia gravis and other neuromuscular disorders. Expert Opin Ther Targets. 21:949–958. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Hettwer S, Lin S, Kucsera S, Haubitz M, Oliveri F, Fariello RG, Ruegg MA and Vrijbloed JW: Injection of a soluble fragment of neural agrin (NT-1654) considerably improves the muscle pathology caused by the disassembly of the neuromuscular junction. PLoS One. 9:e887392014. View Article : Google Scholar : PubMed/NCBI | |
|
Li Z, Li M, Wood K, Hettwer S, Muley SA, Shi FD, Liu Q and Ladha SS: Engineered agrin attenuates the severity of experimental autoimmune myasthenia gravis. Muscle Nerve. 57:814–820. 2018. View Article : Google Scholar : | |
|
Kempermann G, Gage FH, Aigner L, Song H, Curtis MA, Thuret S, Kuhn HG, Jessberger S, Frankland PW, Cameron HA, et al: Human adult neurogenesis: Evidence and remaining questions. Cell Stem Cell. 23:25–30. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D, Kelley KW, James D, Mayer S, Chang J, Auguste KI, et al: Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature. 555:377–381. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Li X, Sun B, Li J, Ye W, Li M, Guan F, Wu S, Luo X, Feng J, Jia J, et al: Sepsis leads to impaired mitochondrial calcium uptake and skeletal muscle weakness by reducing the micu1: Mcu protein ratio. Shock. 60:698–706. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Lv B, Min S, Xie F, Yang J and Chen J: Alleviating sepsis-induced neuromuscular dysfunction linked with acetylcholine receptors by agrin. J Surg Res. 241:308–316. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Abdalla A, Murali C and Amin A: Safranal inhibits angiogenesis via targeting HIF-1α/VEGF machinery: In vitro and Ex vivo insights. Front Oncol. 11:7891722022. View Article : Google Scholar | |
|
Hanahan D and Folkman J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:353–364. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Abdalla Y, Abdalla A, Hamza AA and Amin A: Safranal prevents liver cancer through inhibiting oxidative stress and alleviating inflammation. Front Pharmacol. 12:7775002022. View Article : Google Scholar : PubMed/NCBI | |
|
Bouabdallah S, Al-Maktoum A and Amin A: Steroidal saponins: Naturally occurring compounds as inhibitors of the hallmarks of cancer. Cancers (Basel). 15:39002023. View Article : Google Scholar : PubMed/NCBI | |
|
Wiedmann L, De Angelis Rigotti F, Vaquero-Siguero N, Donato E, Espinet E, Moll I, Alsina-Sanchis E, Bohnenberger H, Fernandez-Florido E, Mulfarth R, et al: HAPLN1 potentiates peritoneal metastasis in pancreatic cancer. Nat Commun. 14:23532023. View Article : Google Scholar : PubMed/NCBI | |
|
He M, Cheng C, Tu J, Ji SS, Lou D and Bai B: Agrin expression is correlated with tumor development and poor prognosis in cholangiocarcinoma. J Int Med Res. 49:30006052110097222021. View Article : Google Scholar : PubMed/NCBI | |
|
Chakraborty S, Lakshmanan M, Swa HL, Chen J, Zhang X, Ong YS, Loo LS, Akincilar SC, Gunaratne J, Tergaonkar V, et al: An oncogenic role of agrin in regulating focal adhesion integrity in hepatocellular carcinoma. Nat Commun. 6:61842015. View Article : Google Scholar : PubMed/NCBI | |
|
Chakraborty S, Njah K, Pobbati AV, Lim YB, Raju A, Lakshmanan M, Tergaonkar V, Lim CT and Hong W: Agrin as a mechanotransduction signal regulating YAP through the hippo pathway. Cell Rep. 18:2464–2479. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Njah K, Chakraborty S, Qiu B, Arumugam S, Raju A, Pobbati AV, Lakshmanan M, Tergaonkar V, Thibault G, Wang X and Hong W: A role of agrin in maintaining the stability of vascular endothelial growth factor receptor-2 during tumor angiogenesis. Cell Rep. 28:949–965.e7. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Bordeleau F, Mason BN, Lollis EM, Mazzola M, Zanotelli MR, Somasegar S, Califano JP, Montague C, LaValley DJ, Huynh J, et al: Matrix stiffening promotes a tumor vasculature phenotype. Proc Natl Acad Sci USA. 114:492–497. 2017. View Article : Google Scholar : | |
|
Frye M, Taddei A, Dierkes C, Martinez-Corral I, Fielden M, Ortsater H, Kazenwadel J, Calado DP, Ostergaard P, Salminen M, et al: Matrix stiffness controls lymphatic vessel formation through regulation of a GATA2-dependent transcriptional program. Nat Commun. 9:15112018. View Article : Google Scholar : PubMed/NCBI | |
|
Chakraborty S, Njah K and Hong W: Agrin mediates angiogenesis in the tumor microenvironment. Trends Cancer. 6:81–85. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Kawahara R, Granato DC, Carnielli CM, Cervigne NK, Oliveria CE, Rivera C, Yokoo S, Fonseca FP, Lopes M, Santos-Silva AR, et al: Agrin and perlecan mediate tumorigenic processes in oral squamous cell carcinoma. PLoS One. 9:e1150042014. View Article : Google Scholar : PubMed/NCBI | |
|
Neill T, Schaefer L and Iozzo RV: Decoding the matrix: Instructive roles of proteoglycan receptors. Biochemistry. 54:4583–4598. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Scherbakov N, Knops M, Ebner N, Valentova M, Sandek A, Grittner U, Dahinden P, Hettwer S, Schefold JC, von Haehling S, et al: Evaluation of C-terminal agrin fragment as a marker of muscle wasting in patients after acute stroke during early rehabilitation. J Cachexia Sarcopenia Muscle. 7:60–67. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Yu D, Li HX, Liu Y, Ying ZW, Guo JJ, Cao CY, Wang J, Li YF and Yang HR: The reference intervals for serum C-terminal agrin fragment in healthy individuals and as a biomarker for renal function in kidney transplant recipients. J Clin Lab Anal. 31:e220592017. View Article : Google Scholar | |
|
Sartori R, Hagg A, Zampieri S, Armani A, Winbanks CE, Viana LR, Haidar M, Watt KI, Qian H, Pezzini C, et al: Perturbed BMP signaling and denervation promote muscle wasting in cancer cachexia. Sci Transl Med. 13:eaay95922021. View Article : Google Scholar : PubMed/NCBI | |
|
Rivera C, Zandonadi FS, Sanchez-Romero C, Soares CD, Granato DC, Gonzalez-Arriagada WA and Paes Leme AF: Agrin has a pathological role in the progression of oral cancer. Br J Cancer. 118:1628–1638. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Bezakova G and Ruegg MA: New insights into the roles of agrin. Nat Rev Mol Cell Biol. 4:295–308. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Sulzmaier FJ, Jean C and Schlaepfer DD: FAK in cancer: Mechanistic findings and clinical applications. Nat Rev Cancer. 14:598–610. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Li D, Gu Q, Xie Z, Shen Q and Li H: Clinical significance of nuclear localisation of agrin in lung adenocarcinoma. Pol J Pathol. 70:198–204. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang QJ, Wan L and Xu HF: High expression of agrin is associated with tumor progression and poor prognosis in hepatocellular carcinoma. Math Biosci Eng. 16:7375–7383. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Ye P, Fu Z, Chung JY, Cao X, Ko H, Tian XY, Tang PM and Lui KO: Endothelial agrin is dispensable for normal and tumor angiogenesis. Front Cardiovasc Med. 8:8104772022. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu Y, Do VD, Richards AM and Foo R: What we know about cardiomyocyte dedifferentiation. J Mol Cell Cardiol. 152:80–91. 2021. View Article : Google Scholar | |
|
Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN and Sadek HA: Transient regenerative potential of the neonatal mouse heart. Science. 331:1078–1080. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zlatanova I, Sun F, Wu RS, Chen X, Lau BH, Colombier P, Sinha T, Celona B, Xu SM, Materna SC, et al: An injury-responsive mmp14b enhancer is required for heart regeneration. Sci Adv. 9:eadh53132023. View Article : Google Scholar : PubMed/NCBI | |
|
Baehr A, Umansky KB, Bassat E, Jurisch V, Klett K, Bozoglu T, Hornaschewitz N, Solyanik O, Kain D, Ferraro B, et al: Agrin promotes coordinated therapeutic processes leading to improved cardiac repair in pigs. Circulation. 142:868–881. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Mazzon C, Anselmo A, Cibella J, Soldani C, Destro A, Kim N, Roncalli M, Burden SJ, Dustin ML, Sarukhan A and Viola A: The critical role of agrin in the hematopoietic stem cell niche. Blood. 118:2733–2742. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Burgess RW, Dickman DK, Nunez L, Glass DJ and Sanes JR: Mapping sites responsible for interactions of agrin with neurons. J Neurochem. 83:271–284. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Guadix JA, Orlova VV, Giacomelli E, Bellin M, Ribeiro MC, Mummery CL, Perez-Pomares JM and Passier R: Human pluripotent stem cell differentiation into functional epicardial progenitor cells. Stem Cell Reports. 9:1754–1764. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Germani A, Foglio E, Capogrossi MC, Russo MA and Limana F: Generation of cardiac progenitor cells through epicardial to mesenchymal transition. J Mol Med (Berl). 93:735–748. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Smits AM, Dronkers E and Goumans MJ: The epicardium as a source of multipotent adult cardiac progenitor cells: Their origin, role and fate. Pharmacol Res. 127:129–140. 2018. View Article : Google Scholar | |
|
Jing X, Liu B, Deng S, Du J and She Q: Agrin yes-associated protein promotes the proliferation of epicardial cells. J Cardiovasc Pharmacol. 77:94–99. 2021. View Article : Google Scholar | |
|
Sun K, Guo J, Guo Z, Hou L, Liu H, Hou Y, He J, Guo F and Ye Y: The roles of the hippo-YAP signalling pathway in cartilage and osteoarthritis. Ageing Res Rev. 90:1020152023. View Article : Google Scholar : PubMed/NCBI | |
|
Hou L, Fu W, Liu Y, Wang Q, Wang L and Huang Y: Agrin promotes limbal stem cell proliferation and corneal wound healing through hippo-yap signaling pathway. Invest Ophthalmol Vis Sci. 61:72020. View Article : Google Scholar : PubMed/NCBI | |
|
Manner J, Schlueter J and Brand T: Experimental analyses of the function of the proepicardium using a new microsurgical procedure to induce loss-of-proepicardial-function in chick embryos. Dev Dyn. 233:1454–1463. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Diman NY, Brooks G, Kruithof BP, Elemento O, Seidman JG, Seidman CE, Basson CT and Hatcher CJ: Tbx5 is required for avian and mammalian epicardial formation and coronary vasculogenesis. Circ Res. 115:834–844. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
van Wijk B, Gunst QD, Moorman AF and van den Hoff MJ: Cardiac regeneration from activated epicardium. PLoS One. 7:e446922012. View Article : Google Scholar : PubMed/NCBI | |
|
Lan Y, Pan H, Li C, Banks KM, Sam J, Ding B, Elemento O, Goll MG and Evans T: TETs regulate proepicardial cell migration through extracellular matrix organization during zebrafish cardiogenesis. Cell Rep. 26:720–732.e4. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Missinato MA, Tobita K, Romano N, Carroll JA and Tsang M: Extracellular component hyaluronic acid and its receptor Hmmr are required for epicardial EMT during heart regeneration. Cardiovasc Res. 107:487–498. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JW, Lafeber FP, Baynes JW and TeKoppele JM: Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem. 275:39027–39031. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Erickson CB, Hill R, Pascablo D, Kazakia G, Hansen K and Bahney C: A timeseries analysis of the fracture callus extracellular matrix proteome during bone fracture healing. J Life Sci (Westlake Village). 3:1–30. 2021. | |
|
Hausser HJ, Ruegg MA, Brenner RE and Ksiazek I: Agrin is highly expressed by chondrocytes and is required for normal growth. Histochem Cell Biol. 127:363–374. 2007. View Article : Google Scholar | |
|
Campanelli JT, Ferns M, Hoch W, Rupp F, von Zastrow M, Hall Z and Scheller RH: Agrin: A synaptic basal lamina protein that regulates development of the neuromuscular junction. Cold Spring Harb Symp Quant Biol. 57:461–472. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Eldridge S, Nalesso G, Ismail H, Vicente-Greco K, Kabouridis P, Ramachandran M, Niemeier A, Herz J, Pitzalis C, Perretti M and Dell'Accio F: Agrin mediates chondrocyte homeostasis and requires both LRP4 and α-dystroglycan to enhance cartilage formation in vitro and in vivo. Ann Rheum Dis. 75:1228–1235. 2016. View Article : Google Scholar | |
|
Eldridge SE, Barawi A, Wang H, Roelofs AJ, Kaneva M, Guan Z, Lydon H, Thomas BL, Thorup AS, Fernandez BF, et al: Agrin induces long-term osteochondral regeneration by supporting repair morphogenesis. Sci Transl Med. 12:eaax90862020. View Article : Google Scholar : PubMed/NCBI | |
|
Gentili C and Cancedda R: Cartilage and bone extracellular matrix. Curr Pharm Des. 15:1334–1348. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Grol MW and Lee BH: Gene therapy for repair and regeneration of bone and cartilage. Curr Opin Pharmacol. 40:59–66. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Gomes KDN, Alves APNN, Dutra PGP and Viana GSB: Doxycycline induces bone repair and changes in Wnt signalling. Int J Oral Sci. 9:158–166. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bao Q, Chen S, Qin H, Feng J, Liu H, Liu D, Li A, Shen Y, Zhao Y, Li J and Zong Z: An appropriate Wnt/β-catenin expression level during the remodeling phase is required for improved bone fracture healing in mice. Sci Rep. 7:26952017. View Article : Google Scholar | |
|
Wang T, Zhang X and Bikle DD: Osteogenic Differentiation of Periosteal Cells During Fracture Healing. J Cell Physiol. 232:913–921. 2017. View Article : Google Scholar : | |
|
Ahn Y, Sims C, Murray MJ, Kuhlmann PK, Fuentes-Antras J, Weatherbee SD and Krumlauf R: Multiple modes of Lrp4 function in modulation of Wnt/β-catenin signaling during tooth development. Development. 144:2824–2836. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Houschyar KS, Tapking C, Borrelli MR, Popp D, Duscher D, Maan ZN, Chelliah MP, Li J, Harati K, Wallner C, et al: Wnt pathway in bone repair and regeneration-what do we know so far. Front Cell Dev Biol. 6:1702019. View Article : Google Scholar | |
|
Shen C, Xiong WC and Mei L: LRP4 in neuromuscular junction and bone development and diseases. Bone. 80:101–108. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Souza ATP, Lopes HB, Oliveira FS, Weffort D, Freitas GP, Adolpho LF, Fernandes RR, Rosa AL and Beloti MM: The extracellular matrix protein Agrin is expressed by osteoblasts and contributes to their differentiation. Cell Tissue Res. 386:335–347. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Willadt S, Nash M and Slater C: Age-related changes in the structure and function of mammalian neuromuscular junctions. Ann N Y Acad Sci. 1412:41–53. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Taetzsch T, Tenga MJ and Valdez G: Muscle fibers secrete FGFBP1 to slow degeneration of neuromuscular synapses during aging and progression of ALS. J Neurosci. 37:70–82. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao K, Shen C, Li L, Wu H, Xing G, Dong Z, Jing H, Chen W, Zhang H, Tan Z, et al: Sarcoglycan alpha mitigates neuromuscular junction decline in aged mice by stabilizing LRP4. J Neurosci. 38:8860–8873. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Samuel MA, Valdez G, Tapia JC, Lichtman JW and Sanes JR: Agrin and synaptic laminin are required to maintain adult neuromuscular junctions. PLoS One. 7:e466632012. View Article : Google Scholar : PubMed/NCBI | |
|
Benjumea AM, Curcio CL, Duque G and Gomez F: Dynapenia and sarcopenia as a risk factor for disability in a falls and fractures clinic in older persons. Open Access Maced J Med Sci. 6:344–349. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang X, Zhang W, Wang C, Tao W, Dou Q and Yang Y: Sarcopenia as a predictor of hospitalization among older people: A systematic review and meta-analysis. BMC Geriatr. 18:1882018. View Article : Google Scholar : PubMed/NCBI | |
|
Stephan A, Mateos JM, Kozlov SV, Cinelli P, Kistler AD, Hettwer S, Rulicke T, Streit P, Kunz B and Sonderegger P: Neurotrypsin cleaves agrin locally at the synapse. FASEB J. 22:1861–1873. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Kamiya K, Tachiki T, Sato Y, Kouda K, Kajita E, Tamaki J, Kagamimori S and Iki M: Association between the 110-kDa C-terminal agrin fragment and skeletal muscle decline among community-dwelling older women. J Cachexia Sarcopenia Muscle. 14:2253–2263. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Drey M, Sieber CC, Bauer JM, Uter W, Dahinden P, Fariello RG and Vrijbloed JW; FiAT intervention group: C-terminal Agrin Fragment as a potential marker for sarcopenia caused by degeneration of the neuromuscular junction. Exp Gerontol. 48:76–80. 2013. View Article : Google Scholar | |
|
Racha P, Selvam S, Bose B, Bantwal G and Sambashivaiah S: Circulating C-terminal agrin fragment: A potential marker for sarcopenia among type 2 diabetes. Indian J Endocrinol Metab. 26:334–340. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Pratt J, De Vito G, Narici M, Segurado R, Pessanha L, Dolan J, Conroy J and Boreham C: Plasma C-terminal agrin fragment as an early biomarker for sarcopenia: Results from the GenoFit study. J Gerontol A Biol Sci Med Sci. 76:2090–2096. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Denzer AJ, Brandenberger R, Gesemann M, Chiquet M and Ruegg MA: Agrin binds to the nerve-muscle basal lamina via laminin. J Cell Biol. 137:671–683. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Denzer AJ, Schulthess T, Fauser C, Schumacher B, Kammerer RA, Engel J and Ruegg MA: Electron microscopic structure of agrin and mapping of its binding site in laminin-1. EMBO J. 17:335–343. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Raats CJ, van den Born J, Bakker MA, Oppers-Walgreen B, Pisa BJ, Dijkman HB, Assmann KJ and Berden JH: Expression of agrin, dystroglycan, and utrophin in normal renal tissue and in experimental glomerulopathies. Am J Pathol. 156:1749–1765. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Goldberg S, Harvey SJ, Cunningham J, Tryggvason K and Miner JH: Glomerular filtration is normal in the absence of both agrin and perlecan-heparan sulfate from the glomerular basement membrane. Nephrol Dial Transplant. 24:2044–2051. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Harvey SJ, Jarad G, Cunningham J, Rops AL, van der Vlag J, Berden JH, Moeller MJ, Holzman LB, Burgess RW and Miner JH: Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol. 171:139–152. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Vestentoft PS, Jelnes P, Andersen JB, Tran TA, Jorgensen T, Rasmussen M, Bornholdt J, Grovdal LM, Jensen CH, Vogel LK, et al: Molecular constituents of the extracellular matrix in rat liver mounting a hepatic progenitor cell response for tissue repair. Fibrogenesis Tissue Repair. 6:212013. View Article : Google Scholar : PubMed/NCBI | |
|
Deng SX, Borderie V, Chan CC, Dana R, Figueiredo FC, Gomes JAP, Pellegrini G, Shimmura S and Kruse FE; The International Limbal Stem Cell Deficiency Working Group: Global consensus on definition, classification, diagnosis, and staging of limbal stem cell deficiency. Cornea. 38:364–375. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Kolli S, Ahmad S, Lako M and Figueiredo F: Successful clinical implementation of corneal epithelial stem cell therapy for treatment of unilateral limbal stem cell deficiency. Stem Cells. 28:597–610. 2010. View Article : Google Scholar | |
|
Whitcher JP, Srinivasan M and Upadhyay MP: Corneal blindness: A global perspective. Bull World Health Organ. 79:214–221. 2001.PubMed/NCBI | |
|
Sacchetti M, Rama P, Bruscolini A and Lambiase A: Limbal stem cell transplantation: Clinical results, limits, and perspectives. Stem Cells Int. 2018:80862692018. View Article : Google Scholar : PubMed/NCBI | |
|
Ribatti D and d'Amati A: Hematopoiesis and Mast Cell Development. Int J Mol Sci. 24:106792023. View Article : Google Scholar : PubMed/NCBI | |
|
Bruno E, Luikart SD, Long MW and Hoffman R: Marrow-derived heparan sulfate proteoglycan mediates the adhesion of hematopoietic progenitor cells to cytokines. Exp Hematol. 23:1212–1217. 1995.PubMed/NCBI | |
|
Sorg H and Sorg CGG: Skin wound healing: Of players, patterns, and processes. Eur Surg Res. 64:141–157. 2023. View Article : Google Scholar | |
|
Xue M and Jackson CJ: Extracellular matrix reorganization during wound healing and its impact on abnormal scarring. Adv Wound Care (New Rochelle). 4:119–136. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Chakraborty S, Sampath D, Yu Lin MO, Bilton M, Huang CK, Nai MH, Njah K, Goy PA, Wang CC, Guccione E, et al: Agrin-matrix metalloproteinase-12 axis confers a mechanically competent microenvironment in skin wound healing. Nat Commun. 12:63492021. View Article : Google Scholar : PubMed/NCBI | |
|
Yu Lin MO, Sampath D, Bosykh DA, Wang C, Wang X, Subramaniam T, Han W, Hong W and Chakraborty S: YAP/TAZ drive agrin-matrix metalloproteinase-12 mediated diabetic skin wound healing. J Invest Dermatol. May 27–2024.Epub ahead of print. View Article : Google Scholar | |
|
Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, Harrington K, Williamson P, Moeendarbary E, Charras G and Sahai E: Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol. 637–646. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Sun X, Malandraki-Miller S, Kennedy T, Bassat E, Klaourakis K, Zhao J, Gamen E, Vieira JM, Tzahor E and Riley PR: The extracellular matrix protein agrin is essential for epicardial epithelial-to-mesenchymal transition during heart development. Development. 148:dev1975252021. View Article : Google Scholar : PubMed/NCBI |
