Origin of tendon stem cells in situ

Tyler Harvey, Chen-Ming Fan

PDF(298 KB)
PDF(298 KB)
Front. Biol. ›› 2018, Vol. 13 ›› Issue (4) : 263-276. DOI: 10.1007/s11515-018-1504-4
REVIEW
REVIEW

Origin of tendon stem cells in situ

Author information +
History +

Abstract

BACKGROUND: Adult stem cells are surveillance repositories capable of supplying a renewable source of progenitors for tissue repair and regeneration to maintain tissue homeostasis throughout life. Many tissue-resident stem cells have been identified in situ, which lays the foundation for studying them in their native microenvironment, i.e. the niche. Within the musculoskeletal system, muscle stem cells have been unequivocally identified in the mouse, which have led to considerable advances in understanding their role in muscle homeostasis and regeneration. On the other hand, for bone and tendon progenitor cells, mesenchymal stem cells have been used as the main in vitro cell model as they can differentiate into osteogenic, chondrogenic and tenogenic fates. Despite considerable efforts and employment of modern tools, the in vivo origins of bone and tendon stem cells remain debated. Tendon regeneration via stem cells is understudied and deserves attention as tendon damage is noted for a bleak, time-consuming recovery and the repaired tendon seldom regains the structural integrity and strength of the native, uninjured state.

OBJECTIVE: Here we review the past efforts and recent studies toward defining adult tendon stem cells and understanding tendon regeneration instead of tendon development. The focus is on adult tendon resident cells in situ and the uncertainty of their roles in regeneration.

METHODS: A systematic literature search using the Pubmed search engine was conducted encompassing the seminal papers in the tendon field.

CONCLUSIONS: Investigation of tendon stem cells in situ is in its infancy mainly due to lack of necessary tools and standardized injury model. We propose a concerted effort toward establishing a comprehensive cell atlas of the tendon, making genetic tools and choosing a reliable injury model for coordinated studies among different laboratories. Increasing our basic understanding should aid future therapeutic innovations to shorten and enhance the tendon repair/regeneration process.

Keywords

Tendon / stem cells / midsubstance / sheath / injury

Cite this article

Download citation ▾
Tyler Harvey, Chen-Ming Fan. Origin of tendon stem cells in situ. Front. Biol., 2018, 13(4): 263‒276 https://doi.org/10.1007/s11515-018-1504-4

References

[1]
Agarwal S, Loder S J, Cholok D, Peterson J, Li J, Breuler C, Cameron Brownley R, Hsin Sung H, Chung M T, Kamiya N, Li S, Zhao B, Kaartinen V, Davis T A, Qureshi A T, Schipani E, Mishina Y, Levi B (2017). Scleraxis-lineage cells contribute to ectopic bone formation in muscle and tendon. Stem Cells, 35(3): 705–710
CrossRef Pubmed Google scholar
[2]
Anderson D M, Arredondo J, Hahn K, Valente G, Martin J F, Wilson-Rawls J, Rawls A (2006). Mohawk is a novel homeobox gene expressed in the developing mouse embryo. Dev Dyn, 235(3): 792–801
CrossRef Pubmed Google scholar
[3]
Arble J R, Lalley A L, Dyment N A, Joshi P, Shin D G, Gooch C, Grawe B, Rowe D, Shearn J T (2016). The LG/J murine strain exhibits near-normal tendon biomechanical properties following a full-length central patellar tendon defect. Connect Tissue Res, 57(6): 496–506
CrossRef Pubmed Google scholar
[4]
Ateschrang A, Ahmad S S, Stöckle U, Schroeter S, Schenk S, Ahrend M D (2017). Recovery of ACL function after dynamic intraligamentary stabilization is resultant to restoration of ACL integrity and scar tissue formation. Knee Surg Sports Tramatol Arthrosc
CrossRef Google scholar
[5]
Bagchi R A and Czubryt M P (2012). Synergistic roles of scleraxis and Smads in the regulation of collagen 1a2 gene expression. Biochim Biophys Acta, 1823(10): 1936–1944
CrossRef Pubmed Google scholar
[6]
Bajpai V K, Mistriotis P, Andreadis S T (2012). Clonal multipotency and effect of long-term in vitro expansion on differentiation potential of human hair follicle derived mesenchymal stem cells. Stem Cell Res (Amst), 8(1): 74–84
CrossRef Pubmed Google scholar
[7]
Baksh N, Hannon C P, Murawski C D, Smyth N A, Kennedy J G (2013). Platelet-rich plasma in tendon models: a systematic review of basic science literature. Arthroscopy, 29(3): 596–607
CrossRef Pubmed Google scholar
[8]
Bao Z Z, Lakonishok M, Kaufman S, Horwitz A F (1993). Alpha 7 beta 1 integrin is a component of the myotendinous junction on skeletal muscle. J Cell Sci, 106(Pt 2): 579–589
Pubmed
[9]
Barker N, van Es J H, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters P J, Clevers H (2007). Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature, 449(7165): 1003–1007
CrossRef Pubmed Google scholar
[10]
Beason D P, Kuntz A F, Hsu J E, Miller K S, Soslowsky L J (2012). Development and evaluation of multiple tendon injury models in the mouse. J Biomech, 45(8): 1550–1553
CrossRef Pubmed Google scholar
[11]
Benjamin M and Ralphs J R (1998). Fibrocartilage in tendons and ligaments--an adaptation to compressive load. J Anat, 193(4): 481–494
CrossRef Pubmed Google scholar
[12]
Berthet E, Chen C, Butcher K, Schneider R A, Alliston T, Amirtharajah M (2013). Smad3 binds Scleraxis and Mohawk and regulates tendon matrix organization. J Orthop Res, 31(9): 1475–1483
CrossRef Pubmed Google scholar
[13]
Bi Y, Ehirchiou D, Kilts T M, Inkson C A, Embree M C, Sonoyama W, Li L, Leet A I, Seo B M, Zhang L, Shi S, Young M F (2007). Identification of tendon stem/progenitor cells and the role of the extracellular matrix in their niche. Nat Med, 13(10): 1219–1227
CrossRef Pubmed Google scholar
[14]
Brent A E, Schweitzer R, Tabin C J (2003). A somitic compartment of tendon progenitors. Cell, 113(2): 235–248
CrossRef Pubmed Google scholar
[15]
Brent A E, Tabin C J (2004). FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development, 131(16): 3885–3896
CrossRef Pubmed Google scholar
[16]
Buschmann J, Bürgisser G M ( 2017). Biomechanics on tendons and ligaments. Zurich: Elsevier, Print
[17]
Cairns J (1975). Mutation selection and the natural history of cancer. Nature, 255(5505): 197–200
CrossRef Pubmed Google scholar
[18]
Calve S, Dennis R G, Kosnik P E 2nd, Baar K, Grosh K, Arruda E M (2004). Engineering of functional tendon. Tissue Eng, 10(5-6): 755–761
CrossRef Pubmed Google scholar
[19]
Chan B P, Fu S, Qin L, Lee K, Rolf C G, Chan K (2000). Effects of basic fibroblast growth factor (bFGF) on early stages of tendon healing: a rat patellar tendon model. Acta Orthop Scand, 71(5): 513–518
CrossRef Pubmed Google scholar
[20]
Chang J, Thunder R, Most D, Longaker M T, Lineaweaver W C (2000). Studies in flexor tendon wound healing: neutralizing antibody to TGF-beta1 increases postoperative range of motion. Plast Reconstr Surg, 105(1): 148–155
CrossRef Pubmed Google scholar
[21]
Charvet B, Ruggiero F, Le Guellec D (2012). The development of the myotendinous junction. A review. Muscles Ligaments Tendons J, 2(2): 53–63
Pubmed
[22]
Chien C, Pryce B, Tufa S F, Keene D R, Huang A H (2017). Optimizing a 3D model system for molecular manipulation of tenogenesis. Connect Tissue Res, 22: 1–14
CrossRef Pubmed Google scholar
[23]
Covas D T, Panepucci R A, Fontes A M, Silva W A Jr, Orellana M D, Freitas M C, Neder L, Santos A R, Peres L C, Jamur M C, Zago M A (2008). Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol, 36(5): 642–654
CrossRef Pubmed Google scholar
[24]
Cserjesi P, Brown D, Ligon K L, Lyons G E, Copeland N G, Gilbert D J, Jenkins N A, Olson E N (1995). Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development, 121(4): 1099–1110
Pubmed
[25]
Dahlgren L A, van der Meulen M C, Bertram J E, Starrak G S, Nixon A J (2002). Insulin-like growth factor-I improves cellular and molecular aspects of healing in a collagenase-induced model of flexor tendinitis. J Orthop Res, 20(5): 910–919
CrossRef Pubmed Google scholar
[26]
Dorrell C, Erker L, Schug J, Kopp J L, Canaday P S, Fox A J, Smirnova O, Duncan A W, Finegold M J, Sander M, Kaestner K H, Grompe M (2011). Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes Dev, 25(11): 1193–1203
CrossRef Pubmed Google scholar
[27]
Dyment N A, Breidenbach A P, Schwartz A G, Russell R P, Aschbacher-Smith L, Liu H, Hagiwara Y, Jiang R, Thomopoulos S, Butler D L, Rowe D W (2015). Gdf5 progenitors give rise to fibrocartilage cells that mineralize via hedgehog signaling to form the zonal enthesis. Dev Biol, 405(1): 96–107
CrossRef Pubmed Google scholar
[28]
Dyment N A, Hagiwara Y, Matthews B G, Li Y, Kalajzic I, Rowe D W (2014). Lineage tracing of resident tendon progenitor cells during growth and natural healing. PLoS One, 9(4): e96113
CrossRef Pubmed Google scholar
[29]
Edom-Vovard F, Duprez D (2004). Signals regulating tendon formation during chick embryonic development. Dev Dyn, 229(3): 449–457
CrossRef Pubmed Google scholar
[30]
Elliott D H (1965). Structure and Function of Mammalian Tendon. Biol Rev Camb Philos Soc, 40(3): 392–421
CrossRef Pubmed Google scholar
[31]
Feil R, Wagner J, Metzger D, Chambon P (1997). Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun, 237(3): 752–757
CrossRef Pubmed Google scholar
[32]
Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D, Chambon P (1996). Ligand-activated site-specific recombination in mice. PNAS 93: 10887–10890
Pubmed
[33]
Franchi M, Trirè A, Quaranta M, Orsini E, Ottani V (2007). Collagen structure of tendon relates to function. Sci World J, 7: 404–420
CrossRef Pubmed Google scholar
[34]
Frolova E G, Drazba J, Krukovets I, Kostenko V, Blech L, Harry C, Vasanji A, Drumm C, Sul P, Jenniskens G J, Plow E F, Stenina-Adognravi O (2014). Control of organization and function of muscle and tendon by thrombospondin-4. Matrix Biol, 37: 35–48
CrossRef Pubmed Google scholar
[35]
Fukui N, Katsuragawa Y, Sakai H, Oda H, Nakamura K (1998). Effect of local application of basic fibroblast growth factor on ligament healing in rabbits. Rev Rhum Engl Ed, 65(6): 406–414
Pubmed
[36]
Gaut L, Duprez D (2016). Tendon development and diseases. Dev Biol, 5(1): 5–23
CrossRef Pubmed Google scholar
[37]
Gaut L, Robert N, Delalande A, Bonnin M A, Pichon C, Duprez D (2016). EGR1 regulates transcription downstream of mechanical signals during tendon formation and healing. PLoS One, 11(11): e0166237
CrossRef Pubmed Google scholar
[38]
Gjorevski N, Sachs N, Manfrin A, Giger S, Bragina M E, Ordóñez-Morán P, Clevers H, Lutolf M P (2016). Designer matrices for intestinal stem cell and organoid culture. Nature, 539(7630): 560–564
CrossRef Pubmed Google scholar
[39]
Grcevic D, Pejda S, Matthews B G, Repic D, Wang L, Li H, Kronenberg M S, Jiang X, Maye P, Adams D J, Rowe D W, Aguila H L, Kalajzic I (2012). In vivo fate mapping identifies mesenchymal progenitor cells. Stem Cells, 30(2): 187–196
CrossRef Pubmed Google scholar
[40]
Guerquin M J, Charvet B, Nourissat G, Havis E, Ronsin O, Bonnin M A, Ruggiu M, Olivera-Martinez I, Robert N, Lu Y, Kadler K E, Baumberger T, Doursounian L, Berenbaum F, Duprez D (2013). Transcription factor EGR1 directs tendon differentiation and promotes tendon repair. J Clin Invest, 123(8): 3564–3576
CrossRef Pubmed Google scholar
[41]
Gumucio J P, Phan A C, Ruehlmann D G, Noah A C, Mendias C L (2014). Synergist ablation induces rapid tendon growth through the synthesis of a neotendon matrix. J Appl Physiol (1985), 117(11): 1287–1291
CrossRef Pubmed Google scholar
[42]
Hall T E, Bryson-Richardson R J, Berger S, Jacoby A S, Cole N J, Hollway G E, Berger J, Currie P D (2007). The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin 2-deficient congenital muscular dystrophy. Proc Natl Acad Sci USA, 104(17): 7092–7
CrossRef Pubmed Google scholar
[43]
Hexter A T, Pendegrass C, Haddad F, Blunn G (2017). Demineralized Bone Matrix to Augment Tendon-Bone Healing: A Systematic Review. Orthop J Sports Med, 5(10): 2325967117734517
CrossRef Pubmed Google scholar
[44]
Hildebrand K A, Woo S L, Smith D W, Allen C R, Deie M, Taylor B J, Schmidt C C (1998). The effects of platelet-derived growth factor-BB on healing of the rabbit medial collateral ligament. An in vivo study. Am J Sports Med, 26(4): 549–554
CrossRef Pubmed Google scholar
[45]
Hoffman P N, Cleveland D W (1988). Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: induction of a specific b-tubulin isotype. Proc Natl Acad Sci USA, 85(12): 4530–4533
CrossRef Pubmed Google scholar
[46]
Howell K, Chien C, Bell R, Laudier D, Tufa S F, Keene D R, Andarawis-Puri N, Huang A H (2017) Novel model of tendon regeneration reveals distinct cell mechanisms underlying regenerative and fibrotic tendon healing. Sci Rep, 7: 45238
CrossRef Google scholar
[47]
Huang A H, Lu H H, Schweitzer R (2015). Molecular regulation of tendon cell fate during development. J Orthop Res, 33(6): 800–812
CrossRef Pubmed Google scholar
[48]
Ibraghimov-Beskrovnaya O, Ervasti J M, Leveille C J, Slaughter C A, Sernett S W, Campbell K P (1992). Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature, 355(6362): 696–702
CrossRef Pubmed Google scholar
[49]
Imokawa Y, Yoshizato K (1997). Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds. Proc Natl Acad Sci USA, 94(17): 9159–9164
CrossRef Pubmed Google scholar
[50]
Ito Y, Toriuchi N, Yoshitaka T, Ueno-Kudoh H, Sato T, Yokoyama S, Nishida K, Akimoto T, Takahashi M, Miyaki S, Asahara H (2010). The Mohawk homeobox gene is a critical regulator of tendon differentiation. Proc Natl Acad Sci USA, 107(23): 10538–10542
CrossRef Pubmed Google scholar
[51]
Ivkovic S, Yoon B S, Popoff S N, Safadi F F, Libuda D E, Stephenson R C, Daluiski A, Lyons K M (2003). Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development, 130(12): 2779–2791
CrossRef Pubmed Google scholar
[52]
Kajikawa Y, Morihara T, Sakamoto H, Matsuda K, Oshima Y, Yoshida A, Nagae M, Arai Y, Kawata M, Kubo T (2008). Platelet-rich plasma enhances the initial mobilization of circulation-derived cells for tendon healing. J Cell Physiol, 215(3): 837–845
CrossRef Pubmed Google scholar
[53]
Kaux J F, Janssen L, Drion P, Nusgens B, Libertiaux V, Pascon F, Heyeres A, Hoffmann A, Lambert C, Le Goff C, Denoël V, Defraigne J O, Rickert M, Crielaard J M, Colige A (2014). Vascular Endothelial Growth Factor-111 (VEGF-111) and tendon healing: preliminary results in a rat model of tendon injury. Muscles Ligaments Tendons J, 4(1): 24–28
Pubmed
[54]
Kirkendall D T and Garrett W E (1997). Function and biomechanics of tendons. Scand J Med Sci Sports, 7(2): 62–66
CrossRef Pubmed Google scholar
[55]
Kretzschmar K and Watt F M (2012). Lineage tracing. Cell, 148(1-2): 33–45
CrossRef Pubmed Google scholar
[56]
Kurth T B, Dell’Accio F, Crouch V, Augello A, Sharpe P T, De Bari C (2011). Functional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo. Arthritis Rheum, 63(5): 1289–1300
CrossRef Google scholar
[57]
Kurtz C A, Loebig T G, Anderson D D, DeMeo P J, Campbell P G (1999). Insulin-like growth factor I accelerates functional recovery from Achilles tendon injury in a rat model. Am J Sports Med, 27(3): 363–369
CrossRef Pubmed Google scholar
[58]
Lalley A L, Dyment N A, Kazemi N, Kenter K, Gooch C, Rowe D W, Butler D L, Shearn J T (2015). Improved biomechanical and biological outcomes in the MRL/MpJ murine strain following a full-length patellar tendon injury. J Orthop Res, 33(11): 1693–1703
CrossRef Pubmed Google scholar
[59]
Lee C H, Lee F Y, Tarafder S, Kao K, Jun Y, Yang G, Mao J J (2015). Harnessing endogenous stem/progenitor cells for tendon regeneration. J Clin Invest, 125(7): 2690–2701
CrossRef Pubmed Google scholar
[60]
Léjard V, Blais F, Guerquin M J, Bonnet A, Bonnin M A, Havis E, Malbouyres M, Bidaud C B, Maro G, Gilardi-Hebenstreit P, Rossert J, Ruggiero F, Duprez D (2011). EGR1 and EGR2 involvement in vertebrate tendon differentiation. J Biol Chem, 286(7): 5855–5867
CrossRef Pubmed Google scholar
[61]
Léjard V, Brideau G, Blais F, Salingcarnboriboon R, Wagner G, Roehrl M H, Noda M, Duprez D, Houillier P, Rossert J (2007). Scleraxis and NFATc regulate the expression of the pro-a1(I) collagen gene in tendon fibroblasts. J Biol Chem, 282(24): 17665–17675
CrossRef Pubmed Google scholar
[62]
Leong D J, Sun H B (2016). Mesenchymal stem cells in tendon repair and regeneration: basic understanding and translational challenges. Ann N Y Acad Sci, 1383(1): 88–96
CrossRef Pubmed Google scholar
[63]
Letson A K, Dahners L E (1994). The effect of combinations of growth factors on ligament healing. Clin Orthop Relat Res, (308): 207–212
Pubmed
[64]
Levay A K, Peacock J D, Lu Y, Koch M, Hinton R B Jr, Kadler K E, Lincoln J (2008). Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ Res, 103(9): 948–956
CrossRef Pubmed Google scholar
[65]
Li L and Clevers H (2010). Coexistence of quiescent and active adult stem cells in mammals. Science, 327(5965): 542–545
CrossRef Pubmed Google scholar
[66]
Lin T W, Cardenas L, Glaser D L, Soslowsky L J (2006). Tendon healing in interleukin-4 and interleukin-6 knockout mice. J Biomech, 39(1): 61–69
CrossRef Pubmed Google scholar
[67]
Liu C F, Aschbacher-Smith L, Barthelery N J, Dyment N, Butler D, and Wylie C (2012). Spatial and temporal expression of molecular markers and cell signals during normal development of the mouse patellar tendon. Tissue Eng Part A, 18(5-6): 598–608
CrossRef Pubmed Google scholar
[68]
Liu H, Xu J, Liu C F, Lan Y, Wylie C, Jiang R (2015). Whole transcriptome expression profiling of mouse limb tendon development by using RNA-seq. J Orthop Res, 33(6): 840–848
CrossRef Pubmed Google scholar
[69]
Liu R, Zhang Z, Xu Y (2010). Downregulation of nucleostemin causes G1 cell cycle arrest via a p53-independent pathway in prostate cancer PC-3 cells. Urol Int, 85(2): 221–227
CrossRef Pubmed Google scholar
[70]
Liu Z, Martin L J (2003). Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J Comp Neurol, 459(4): 368–391
CrossRef Pubmed Google scholar
[71]
Lu H H, Thomopoulos S (2013). Functional attachment of soft tissues to bone: development, healing, and tissue engineering. Annu Rev Biomed Eng, 15(1): 201–226
CrossRef Pubmed Google scholar
[72]
Lui P, Zhang P, Chan K, Qin L (2010). Biology and augmentation of tendon-bone insertion repair. J Orthop Surg, 5(1): 59
CrossRef Pubmed Google scholar
[73]
Lyras D N, Kazakos K, Verettas D, Botaitis S, Agrogiannis G, Kokka A, Pitiakoudis M, Kotzakaris A (2009). The effect of platelet-rich plasma gel in the early phase of patellar tendon healing. Arch Orthop Trauma Surg, 129(11): 1577–1582
CrossRef Pubmed Google scholar
[74]
Maeda T, Sakabe T, Sunaga A, Sakai K, Rivera A L, Keene D R, Sasaki T, Stavnezer E, Iannotti J, Schweitzer R, Ilic D, Baskaran H, Sakai T (2011). Conversion of mechanical force into TGF-b-mediated biochemical signals. Curr Biol, 21(11): 933–941
CrossRef Pubmed Google scholar
[75]
Mendias C L, Gumucio J P, Bakhurin K I, Lynch E B, Brooks S V (2012). Physiological loading of tendons induces scleraxis expression in epitenon fibroblasts. J Orthop Res, 30(4): 606–612
CrossRef Pubmed Google scholar
[76]
Miosge N, Klenczar C, Herken R, Willem M, Mayer U (1999). Organization of the myotendinous junction is dependent on the presence of alpha7beta1 integrin. Lab Invest, 79(12): 1591–1599
Pubmed
[77]
Molloy T, Wang Y, Murrell G (2003). The roles of growth factors in tendon and ligament healing. Sports Med, 33(5): 381–394
CrossRef Pubmed Google scholar
[78]
Murchison N D, Price B A, Conner D A, Keene D R, Olson E N, Tabin C J, Schweitzer R (2007). Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development, 134: 2697–2708
CrossRef Google scholar
[79]
Paxton J Z, Donnelly K, Keatch R P, Baar K (2009). Engineering the bone-ligament interface using polyethylene glycol diacrylate incorporated with hydroxyapatite. Tissue Eng Part A, 15(6): 1201–1209
CrossRef Pubmed Google scholar
[80]
Paxton J Z, Grover L M, Baar K (2010). Engineering an in vitro model of a functional ligament from bone to bone. Tissue Eng Part A, 16(11): 3515–3525
CrossRef Pubmed Google scholar
[81]
Perez A V, Perrine M, Brainard N, Vogel K G (2003). Scleraxis (Scx) directs lacZ expression in tendon of transgenic mice. Mech Dev, 120(10): 1153–1163
CrossRef Pubmed Google scholar
[82]
Petersen J R, Agarwal S, Brownley R C, Loder S J, Ranganathan K, Cederna P S, Mishina Y, Wang S C, Levi B (2015). Direct mouse trauma/burn model for heterotopic ossification. J Vis Exp (102): 52880
CrossRef Pubmed Google scholar
[83]
Petersen W, Fink C, Kopf S (2017). Return to sports after ACL reconstruction: a paradigm shift from time to function. Knee Surg Sports Traumatol Arthrosc, 25(5): 1353–1355
CrossRef Pubmed Google scholar
[84]
Potten C S, Hendry J H (1975). Differential regeneration of intestinal proliferative cells and cryptogenic cells after irradiation. Int J Radiat Biol Relat Stud Phys Chem Med, 27(5): 413–424
CrossRef Pubmed Google scholar
[85]
Pryce B A, Brent A E, Murchison N D, Tabin C J, Schweitzer R (2007). Generation of transgenic tendon reporters, ScxGFP and ScxAP, using regulatory elements of the scleraxis gene. Dev Dyn, 236(6): 1677–1682
CrossRef Pubmed Google scholar
[86]
Pryce B A, Watson S S, Murchison N D, Staverosky J A, Dünker N, Schweitzer R (2009). Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development, 136(8): 1351–1361
CrossRef Pubmed Google scholar
[87]
Rees S G, Waggett A D, Kerr B C, Probert J, Gealy E C, Dent C M, Caterson B, Hughes C E (2009). Immunolocalisation and expression of keratocan in tendon. Osteoarthritis Cartilage, 17(2): 276–279
CrossRef Pubmed Google scholar
[88]
Richardson S H, Starborg T, Lu Y, Humphries S M, Meadows R S, Kadler K E (2007). Tendon development requires regulation of cell condensation and cell shape via cadherin-11-mediated cell-cell junctions. Mol Cell Biol, 27(17): 6218–6228
CrossRef Pubmed Google scholar
[89]
Rickert M, Jung M, Adiyaman M, Richter W, and Simank H G (2001). A growth and differentiation factor-5 (GDF-5)-coated suture stimulates tendon healing in an Achilles tendon model in rats. Growth Factors, 19(2): 115–126
CrossRef Pubmed Google scholar
[90]
Rountree R B, Schoor M, Chen H, Marks M E, Harley V, Mishina Y, Kingsley D M (2004). BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol, 2(11): e355
CrossRef Pubmed Google scholar
[91]
Rubio-Azpeitia E, Sánchez P, Delgado D, Andia I (2015). Three-dimensional platelet rich plasma hydrogel model to study early tendon healing. Cells Tissues Organs, 200(6): 394–404
CrossRef Pubmed Google scholar
[92]
Runesson E, Ackermann P, Brisby H, Karlsson J, Eriksson B I (2013). Detection of slow-cycling and stem/progenitor cells in different regions of rat Achilles tendon: response to treadmill exercise. Knee Surg Sports Traumatol Arthrosc, 21(7): 1694–1703
CrossRef Pubmed Google scholar
[93]
Runesson E, Ackermann P, Karlsson J, Eriksson B I (2015). Nucleostemin- and Oct 3/4-positive stem/progenitor cells exhibit disparate anatomical and temporal expression during rat Achilles tendon healing. BMC Musculoskelet Disord, 16(212): 1
CrossRef Pubmed Google scholar
[94]
Sato T, Vries R G, Snippert H J, van de Wetering M, Barker N, Stange D E, van Es J H, Abo A, Kujala P, Peters P J, Clevers H (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 459(7244): 262–265
CrossRef Pubmed Google scholar
[95]
Schwartz A G, Galatz L M, Thomopoulos S (2017). Enthesis regeneration: a role for Gli1+ progenitor cells. Development, 144(7): 1159–1164
CrossRef Pubmed Google scholar
[96]
Schwartz Y, Viukov S, Krief S, Zelzer E (2016). Joint development involves a continuous influx of Gdf5-positive cells. Cell Reports, 15(12): 2577–2587
CrossRef Pubmed Google scholar
[97]
Schweitzer R, Chyung J H, Murtaugh L C, Brent A E, Rosen V, Olson E N, Lassar A, Tabin C J (2001). Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments. Development, 128(19): 3855–3866
Pubmed
[98]
Shah R R, Nerurkar N L, Wang C C, Galloway J L (2015). Tensile properties of craniofacial tendons in the mature and aged zebrafish. J Orthop Res, 33(6): 867–873
CrossRef Pubmed Google scholar
[99]
Shih I M (1999). The role of CD146 (Mel-CAM) in biology and pathology. J Pathol, 189(1): 4–11
CrossRef Pubmed Google scholar
[100]
Shukunami C, Takimoto A, Oro M, Hiraki Y (2006). Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol, 298(1): 234–247
CrossRef Pubmed Google scholar
[101]
Snippert H J, van der Flier L G, Sato T, van Es J H, van den Born M, Kroon-Veenboer C, Barker N, Klein A M, van Rheenen J, Simons B D, Clevers H (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell, 143(1): 134–144
CrossRef Pubmed Google scholar
[102]
Soriano P (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet, 21(1): 70–71
CrossRef Pubmed Google scholar
[103]
Starborg T, Kalson N S, Lu Y, Mironov A, Cootes T F, Holmes D F, Kadler K E (2013). Using transmission electron microscopy and 3View to determine collagen fibril size and three-dimensional organization. Nat Protoc, 8(7): 1433–1448
CrossRef Pubmed Google scholar
[104]
Staverosky J A, Pryce B A, Watson S S, Schweitzer R (2009). Tubulin polymerization-promoting protein family member 3, Tppp3, is a specific marker of the differentiating tendon sheath and synovial joints. Dev Dyn, 238(3): 685–692
CrossRef Pubmed Google scholar
[105]
Subramanian A and Schilling T F (2014). Thrombospondin-4 controls matrix assembly during development and repair of myotendinous junctions. eLife, 3: e02372
CrossRef Pubmed Google scholar
[106]
Subramanian A and Schilling T F (2015). Tendon development and musculoskeletal assembly: emerging roles for the extracellular matrix. Development, 142(24): 4191–4204
CrossRef Pubmed Google scholar
[107]
Subramanian A, Wayburn B, Bunch T, Volk T (2007). Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development, 134(7): 1269–1278
CrossRef Pubmed Google scholar
[108]
Sugimoto Y, Takimoto A, Hiraki Y, Shukunami C (2013). Generation and characterization of ScxCre transgenic mice. Genesis, 51(4): 275–283
CrossRef Pubmed Google scholar
[109]
Sundar S, Pendegrass C J, Blunn G W (2009). Tendon bone healing can be enhanced by demineralized bone matrix: a functional and histological study. J Biomed Mater Res B Appl Biomater, 88B(1): 115–122
CrossRef Pubmed Google scholar
[110]
Tan Q, Lui P P Y, Lee Y W (2013). In vivo identity of tendon stem cells and the roles of stem cells in tendon healing. Stem Cells Dev, 22(23): 3128–3140
CrossRef Pubmed Google scholar
[111]
Thomopoulos S, Williams G R, Gimbel J A, Favata M, Soslowsky L J (2003). Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. J Orthop Res, 21(3): 413–419
CrossRef Pubmed Google scholar
[112]
Tidball J G, Lin C (1989). Structural changes at the myogenic cell surface during the formation of myotendinous junctions. Cell Tissue Res, 257(1): 77–84
CrossRef Pubmed Google scholar
[113]
Urdzikova L M, Sedlacek R, Suchy T, Amemori T, Ruzicka J, Lesny P, Havlas V, Sykova E, Jendelova P (2014). Human multipotent mesenchymal stem cells improve healing after collagenase tendon injury in the rat. Biomed Eng Online, 13(42): 1–15
CrossRef Pubmed Google scholar
[114]
Veronesi F, Salamanna F, Tschon M, Maglio M, Nicoli Aldini N, Fini M (2017). Mesenchymal stem cells for tendon healing: what is on the horizon? J Tissue Eng Regen Med, 11(11): 3202–3219
CrossRef Pubmed Google scholar
[115]
Wang Y, Zhang X, Huang H, Xia Y, Yao Y, Mak A F, Yung P S, Chan K M, Wang L, Zhang C, Huang Y, Mak K K (2017). Osteocalcin expressing cells from tendon sheaths in mice contribute to tendon repair by activating Hedgehog signaling. eLife, 6: e30474
CrossRef Pubmed Google scholar
[116]
Watson S S, Riordan T J, Pryce B A, Schweitzer R (2009). Tendons and muscles of the mouse forelimb during embryonic development. Dev Dyn, 238(3): 693–700
CrossRef Pubmed Google scholar
[117]
Wolfman N M, Hattersley G, Cox K, Celeste A J, Nelson R, Yamaji N, Dube J L, DiBlasio-Smith E, Nove J, Song J J, Wozney J M, Rosen V (1997). Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J Clin Invest, 100(2): 321–330
CrossRef Pubmed Google scholar
[118]
Wu Y, Wang Z, Ying Hsi Fuh J, San Wong Y, Wang W, San Thian E (2017). Direct E-jet printing of three-dimensional fibrous scaffold for tendon tissue engineering. J Biomed Mater Res B Appl Biomater, 105(3): 616–627
CrossRef Pubmed Google scholar
[119]
Wu Y, Wong Y S, Fuh J Y H (2017). Degradation behaviors of geometric cues and mechanical properties in a 3D scaffold for tendon repair. J Biomed Mater Res A, 105(4): 1138–1149
CrossRef Pubmed Google scholar
[120]
Yin H, Yan Z, Bauer R J, Peng J, Schieker M, Nerlich M, Docheva D (2018). Functionalized thermosensitive hydrogel combined with tendon stem/progenitor cells as injectable cell delivery carrier for tendon tissue engineering. Biomed Mater, 13(3): 034107
CrossRef Pubmed Google scholar
[121]
Yoshimoto Y, Takimoto A, Watanabe H, Hiraki Y, Kondoh G, Shukunami C (2017). Scleraxis is required for maturation of tissue domains for proper integration of the musculoskeletal system. Sci Rep, 7: 1-16
CrossRef Pubmed Google scholar
[122]
Zampeli F, Terzidis I, Espregueiera-Mendes J, Georgoulis J D, Bernard M, Pappas E, Georgoulis A D (2017). Restoring tibiofemoral alignment during ACL reconstruction results in better knee biomechanics. Knee Surg Sports Traumatol Arthrosc, 25(6): 1367-1374
CrossRef Pubmed Google scholar
[123]
Zhang J and Wang J H C (2010). Characterization of differential properties of rabbit tendon stem cells and tenocytes. BMC Musculoskelet Disord, 11(10): 1
CrossRef Pubmed Google scholar
[124]
Zhang Y, Kao W W Y, Hayashi Y, Zhang L, Call M, Dong F, Yuan Y, Zhang J, Wang Y C, Yuka O, Shiraishi A, Liu C Y (2017). Generation and characterization of a novel mouse line, Keratocan-rtTA (KeraRT), for corneal stroma and tendon research. Invest Ophthalmol Vis Sci, 58(11): 4800–4808
CrossRef Pubmed Google scholar
[125]
Zheng G X Y, Terry J M, Belgrader P, Ryvkin P, Bent Z W, Wilson R, Ziraldo S B, Wheeler T D, McDermott G P, Zhu J, Gregory M T, Shuga J, Montesclaros L, Underwood J G, Masquelier D A, Nishimura S Y, Schnall-Levin M, Wyatt P W, Hindson C M, Bharadwaj R, Wong A, Ness K D, Beppu L W, Deeg H J, McFarland C, Loeb K R, Valente W J, Ericson N G, Stevens E A, Radich J P, Mikkelsen T S, Hindson B J, Bielas J H (2017). Massively parallel digital transcriptional profiling of single cells. Nat Commun, 8: 1-12
CrossRef Pubmed Google scholar

Compliance with ethics guidelines

Authors declare no conflict of interest. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

2018 Higher Education Press and Springer-Verlag GmbH, part of Springer Nature
PDF(298 KB)

Accesses

Citations

Detail

Sections
Recommended

/