Bioprinted Notch ligand to function as stem cell niche improves muscle regeneration in dystrophic muscle

Zewei Sun, Xianlin Yue, Lei Liu, Ying Li, Jie Cui, Dong Li, Lee Weiss, Phil Campbell, Yanling Mu, Johnny Huard, Xiaodong Mu

Article ID: 711
Vol 9, Issue 3, 2023, Article identifier:

VIEWS - 71 (Abstract) 47 (PDF)

Abstract


In Duchenne muscular dystrophy, dystrophic muscle phenotypes are closely associated with the exhaustion of muscle stem cells. Transplantation of muscle stem cells has been widely studied for improving muscle regeneration, but poor cell survival and self-renewal, rapid loss of stemness, and limited dispersion of grafted cells following transplantation have collectively hindered the overall success of this strategy. Optimized mechanisms for maintaining and improving stem cell function are naturally present in the microenvironment of the stem cell niche in healthy muscles. Therefore, one logical strategy toward improving stem cell function and efficiency of stem cell transplantation in diseased muscles would be the establishment of a microenvironment mimicking some key aspects of healthy native stem cell niches. Here, we applied inkjet-based bioprinting technology to engineer a mimicked artificial stem cell niche in dystrophic muscle, comprising stem cell niche regulating factors (Notch activator DLL1) bioprinted onto 3D DermaMatrix construct. The recombinant DLL1 protein, DLL1 (mouse): Fc (human) (rec), was applied here as the Notch activator. Bioprinted DermaMatrix construct was seeded with muscle stem cells in vitro, and increased stem cell maintenance and repressed myogenic differentiation process was observed. DLL1 bioprinted DermaMatrix construct was then engrafted into dystrophic muscle of mdx/scid mice, and the improved cell engraftment and progression of muscle regeneration was observed 10 days after engraftment. Our results demonstrated that bioprinting of Notch activator within 3D construct can be applied to serve as muscle stem cell niche and improve the efficacy of muscle stem cell transplantation in diseased muscle


Keywords


Muscle dystrophy, Stem cell niche, Muscle stem cell, Notch signaling

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Sacco A, Mourkioti F, Tran R, et al., 2010, Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell, 143(7):1059–1071. https://doi.org/10.1016/j.cell.2010.11.039

Jang YC, Sinha M, Cerletti M, et al., 2011, Skeletal muscle stem cells: Effects of aging and metabolism on muscle regenerative function. Cold Spring Harb Symp Quant Biol, 76:101–111. https://doi.org/10.1101/sqb.2011.76.010652

Usas A, Maciulaitis J, Maciulaitis R, et al., 2011, Skeletal muscle-derived stem cells: Implications for cell-mediated therapies. Medicina (Kaunas), 47(9):469–479.

Ikezawa M, Cao B, Qu Z, et al., 2003, Dystrophin delivery in dystrophin-deficient DMDmdx skeletal muscle by isogenic muscle-derived stem cell transplantation. Hum Gene Ther, 14(16):1535–1546. https://doi.org/10.1089/104303403322495043

Winkler T, von Roth P, Matziolis G, et al., 2009, Dose-response relationship of mesenchymal stem cell transplantation and functional regeneration after severe skeletal muscle injury in rats. Tissue Eng Part A, 15(3):487–492. https://doi.org/10.1089/ten.tea.2007.0426

Tremblay JP, Malouin F, Roy R, et al., 1993, Results of a triple blind clinical study of myoblast transplantations without immunosuppressive treatment in young boys with Duchenne muscular dystrophy. Cell Transplant, 2(2): 99–112.

Drowley L, Okada M, Beckman S, et al., 2010, Cellular antioxidant levels influence muscle stem cell therapy. Mol Ther, 18(10):1865–1873. https://doi.org/10.1038/mt.2010.160

Maclean S, Khan WS, Malik AA, et al., 2012, The potential of stem cells in the treatment of skeletal muscle injury and disease. Stem Cells Int, 2012:282348. https://doi.org/10.1155/2012/282348

Gussoni E, Blau HM, Kunkel LM, 1997, The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med, 3(9):970–977.

Karpati G, Holland P, Worton RG, 1992, Myoblast transfer in DMD: Problems in the interpretation of efficiency. Muscle Nerve, 15(10):1209–1210. https://doi.org/10.1002/mus.880151016

Mayeuf A, Relaix F, 2011, Notch pathway: From development to regeneration of skeletal muscle. Med Sci (Paris), 27(5):521–526. https://doi.org/10.1051/medsci/2011275018

Carey KA, Farnfield MM, Tarquinio SD, et al., 2007, Impaired expression of Notch signaling genes in aged human skeletal muscle. J Gerontol A Biol Sci Med Sci, 62(1):9–17. https://doi.org/62/1/9

Conboy IM, Rando TA, 2002, The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell, 3(3):397–409.

Acharyya S, Sharma SM, Cheng AS, et al., 2010, TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: Implications in Duchenne muscular dystrophy. PLoS One, 5(8):e12479. https://doi.org/10.1371/journal.pone.0012479

Sweeney C, Morrow D, Birney YA, et al., 2004, Notch 1 and 3 receptor signaling modulates vascular smooth muscle cell growth, apoptosis, and migration via a CBF-1/RBP-Jk dependent pathway. FASEB J, 18(12):1421–1423. https://doi.org/10.1096/fj.04-1700fje04-1700fje

Li Y, Hiroi Y, Liao JK, 2010, Notch signaling as an important mediator of cardiac repair and regeneration after myocardial infarction. Trends Cardiovasc Med, 20(7):228–231. https://doi.org/10.1016/j.tcm.2011.11.006

Carlson ME, Hsu M, Conboy IM, 2008, Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature, 454(7203):528–532. https://doi.org/10.1038/nature07034

Yang K, Proweller A, 2011, Vascular smooth muscle Notch signals regulate endothelial cell sensitivity to angiogenic stimulation. J Biol Chem, 286(15):13741–13753. https://doi.org/10.1074/jbc.M110.181842

Phng LK, Gerhardt H, 2009, Angiogenesis: A team effort coordinated by notch. Dev Cell, 16(2):196–208. https://doi.org/10.1016/j.devcel.2009.01.015

Boonen KJ, Post MJ, 2008, The muscle stem cell niche: Regulation of satellite cells during regeneration. Tissue Eng Part B Rev, 14(4):419–431. https://doi.org/10.1089/ten.teb.2008.0045

Kuang S, Kuroda K, Le Grand F, et al., 2007, Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell, 129(5):999–1010. https://doi.org/10.1016/j.cell.2007.03.044

Chakkalakal JV, Jones KM, Basson MA, et al., 2012, The aged niche disrupts muscle stem cell quiescence. Nature, 490(7420):355–360. https://doi.org/10.1038/nature11438

Bjornson CR, Cheung TH, Liu L, et al., 2012, Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells, 30(2):232–242. https://doi.org/10.1002/stem.773

Mourikis P, Sambasivan R, Castel D, et al., 2012, A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells, 30(2):243–252. https://doi.org/10.1002/stem.775

Fukada S, Yamaguchi M, Kokubo H, et al., 2011, Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development, 138(21):4609–4619. https://doi.org/10.1242/dev.067165

Brohl D, Vasyutina E, Czajkowski MT, et al., 2012, Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals. Dev Cell, 23(3):469–481. https://doi.org/10.1016/j.devcel.2012.07.014

Lepper C, Low S, Partridge TA, 2012, The satellite cell builds its nest under Notch’s guidance. Cell Stem Cell, 11(4):443–444. https://doi.org/10.1016/j.stem.2012.09.010

Vieira NM, Elvers I, Alexander MS, et al., 2015, Jagged 1 rescues the Duchenne muscular dystrophy phenotype. Cell, 163(5):1204–1213. https://doi.org/10.1016/j.cell.2015.10.049

Gharaibeh B, Lu A, Tebbets J, et al., 2008, Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc, 3(9):1501–1509. https://doi.org/10.1038/nprot.2008.142

Ota S, Uehara K, Nozaki M, et al., 2011, Intramuscular transplantation of muscle-derived stem cells accelerates skeletal muscle healing after contusion injury via enhancement of angiogenesis. Am J Sports Med, 39(9):1912– 1922. https://doi.org/10.1177/0363546511415239

Sekiya N, Tobita K, Beckman S, et al., 2013, Muscle-derived stem cell sheets support pump function and prevent cardiac arrhythmias in a model of chronic myocardial infarction. Mol Ther, 21(3):662–9. https://doi.org/10.1038/mt.2012.266

Matai I, Kaur G, Seyedsalehi A, et al., 2020, Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials, 226:119536. https://doi.org/10.1016/j.biomaterials.2019.119536

Vijayavenkataraman S, Yan WC, Lu WF, et al., 2018, 3D bioprinting of tissues and organs for regenerative medicine. Adv Drug Deliv Rev, 132:296–332. https://doi.org/10.1016/j.addr.2018.07.004

Ng WL, Chua CK, Shen Y-F, 2019, Print me an organ! Why we are not there yet. Progr Polym Sci, 97:101145. https://doi.org/10.1016/j.progpolymsci.2019.101145

Ng WL, Lee JM, Zhou M, et al., 2020, Vat polymerization-based bioprinting-process, materials, applications and regulatory challenges. Biofabrication, 12(2):022001. https://doi.org/10.1088/1758-5090/ab6034

Ng WL, Huang X, Shkolnikov V, et al., 2022, Controlling droplet impact velocity and droplet volume: Key factors to achieving high cell viability in sub-nanoliter droplet-based bioprinting. Int J Bioprint, 8(1):424. https://doi.org/10.18063/ijb.v8i1.424

Zhou C, Yang Y, Wang J, et al., 2021, Ferromagnetic soft catheter robots for minimally invasive bioprinting. Nat Commun, 12(1):5072. https://doi.org/10.1038/s41467-021-25386-w

Jiang T, Munguia-Lopez GJ, Flores-Torres S, et al., 2019, Extrusion bioprinting of soft materials: An emerging technique for biological model fabrication. Appl Phys Rev, 6(1):011310. https://doi.org/10.1063/1.5059393, 10.1063/1.5085013, 10.1063/1.5055659, 10.1063/1.5053909

Eisenberg MC, Kim Y, Li R, et al., 2011, Mechanistic modeling of the effects of myoferlin on tumor cell invasion. Proc Natl Acad Sci U S A, 108(50):20078–20083. https://doi.org/10.1073/pnas.1116327108

Yerneni SS, Whiteside TL, Weiss LE, et al., 2019, Bioprinting exosome-like extracellular vesicle microenvironments. Bioprinting, 13:e00041. https://doi.org/10.1016/j.bprint.2019.e00041

Cooper GM, Miller ED, DeCesare GE, et al., 2010, Inkjet-based biopatterning of bone morphogenetic protein-2 to spatially control calvarial bone formation. Tissue Eng Part A, 16:1749–1759. https://doi.org/10.1089/ten.TEA.2009.0650

Ker ED, Nain AS, Weiss LE, et al., 2011, Bioprinting of growth factors onto aligned sub-micron fibrous scaffolds for simultaneous control of cell differentiation and alignment. Biomaterials, 32(32):8097–8107. https://doi.org/10.1016/j.biomaterials.2011.07.025

Herberg S, Kondrikova G, Periyasamy-Thandavan S, et al., 2014, Inkjet-based biopatterning of SDF-1beta augments BMP-2-induced repair of critical size calvarial bone defects in mice. Bone, 67:95–103. https://doi.org/10.1016/j.bone.2014.07.007

Skuk D, Tremblay JP, 2000, Progress in myoblast transplantation: A potential treatment of dystrophies. Microsc Res Tech, 48(3-4):213–222. https://doi.org/10.1002/(SICI)1097-0029(20000201/15)48: 3/4<213::AID-JEMT9>3.0.CO;2-Z

Bouchentouf M, Benabdallah BF, Tremblay JP, 2004, Myoblast survival enhancement and transplantation success improvement by heat-shock treatment in mdx mice. Transplantation, 77(9):1349–1356.

Skuk D, Caron NJ, Goulet M, et al., 2003, Resetting the problem of cell death following muscle-derived cell transplantation: Detection, dynamics and mechanisms. J Neuropathol Exp Neurol, 62(9):951–967.

Qu-Petersen Z, Deasy B, Jankowski R, et al., 2002, Identification of a novel population of muscle stem cells in mice: Potential for muscle regeneration. J Cell Biol, 157(5):851–864. https://doi.org/10.1083/jcb.200108150

Deasy BM, Jankowski RJ, Huard J, 2001, Muscle-derived stem cells: Characterization and potential for cell-mediated therapy. Blood Cells Mol Dis, 27(5):924–933. https://doi.org/10.1006/bcmd.2001.0463

Parker MH, Loretz C, Tyler AE, et al., 2012, Activation of Notch signaling during ex vivo expansion maintains donor muscle cell engraftment. Stem Cells, 30(10):2212–2220. https://doi.org/10.1002/stem.1181




DOI: http://dx.doi.org/10.18063/ijb.711

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