Connecting muscles to tendons: Tendons and musculoskeletal development in flies and vertebrates

Development

Volumn 137, Issue 17, 2010, Pages 2807-2817

  Schweitzer, Ronen ^a,b   Zelzer, Elazar ^c   Volk, Talila ^c  

^a SHRINERS HOSPITAL FOR CHILDREN   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Bone tendon interaction; Drosophila; Muscle tendon interaction; Tendon development; Vertebrate

Indexed keywords

ALPHA7 INTEGRIN; BONE MORPHOGENETIC PROTEIN 4; COLLAGEN TYPE 10; COLLAGEN TYPE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR; LAMININ; MEMBRANE PROTEIN; MYOGENIC FACTOR 5; NOTCH RECEPTOR; PARATHYROID HORMONE RELATED PROTEIN RECEPTOR; SONIC HEDGEHOG PROTEIN; TENOMODULIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR SCLERAXIS; TRANSCRIPTION FACTOR STRIPEB; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT1 PROTEIN;

BONE; BONE GROWTH; CARTILAGE; CELL AGGREGATION; CELL MIGRATION; DERMIS; DROSOPHILA; ECTODERM; EMBRYO DEVELOPMENT; FLY; GENE EXPRESSION; LOCOMOTION; MUSCLE; MUSCULOSKELETAL DEVELOPMENT; MYOBLAST; MYOTOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TENDON; VERTEBRATE; ANIMAL; GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT;

INVERTEBRATA; VERTEBRATA;

ANIMALS; DROSOPHILA; MUSCLES; MUSCULOSKELETAL DEVELOPMENT; SIGNAL TRANSDUCTION; TENDONS; VERTEBRATES;

EID: 77956218581     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.047498     Document Type: Review

References (90)

1. Akiyama, H., Kamitani, T., Yang, X., Kandyil, R., Bridgewater, L. C., Fellous, M., Mori-Akiyama, Y. and de Crombrugghe, B. (2005). The transcription factor Sox9 is degraded by the ubiquitin-proteasome system and stabilized by a mutation in a ubiquitin-target site. Matrix Biol. 23, 499-505. (Pubitemid 40202748)
2. Becker, S., Pasca, G., Strumpf, D., Min, L. and Volk, T. (1997). Reciprocal signaling between Drosophila epidermal muscle attachment cells and their corresponding muscles. Development 124, 2615-2622.
3. Benjamin, M. and Ralphs, J. R. (1997). Tendons and ligaments - an overview. Histol. Histopathol. 12, 1135-1144.
4. Benjamin, M., Kumai, T., Milz, S., Boszczyk, B. M., Boszczyk, A. A. and Ralphs, J. R. (2002). The skeletal attachment of tendons-tendon 'entheses'. Comp. Biochem. Physiol. A Physiol. 133, 931-945.
5. Benjamin, M., Toumi, H., Ralphs, J. R., Bydder, G., Best, T. M. and Milz, S. (2006). Where tendons and ligaments meet bone: attachment sites ('entheses') in relation to exercise and/or mechanical load. J. Anat. 208, 471-490.
6. Benjamin, M., Kaiser, E. and Milz, S. (2008). Structure-function relationships in tendons: a review. J. Anat. 212, 211-228.
7. Biewener, A. A., Fazzalari, N. L., Konieczynski, D. D. and Baudinette, R. V. (1996). Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone 19, 1-8.
8. Blitz, E., Viukov, S., Sharir, A., Shwartz, Y., Galloway, J. L., Pryce, B. A., Johnson, R. L., Tabin, C. J., Schweitzer, R. and Zelzer, E. (2009). Bone ridge patterning during musculoskeletal assembly is mediated through SCX regulation of Bmp4 at the tendon-skeleton junction. Dev. Cell 17, 861-873.
9. Bokel, C. and Brown, N. H. (2002). Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev. Cell 3, 311-321.
10. Bonnin, M. A., Laclef, C., Blaise, R., Eloy-Trinquet, S., Relaix, F., Maire, P. and Duprez, D. (2005). Six1 is not involved in limb tendon development, but is expressed in limb connective tissue under Shh regulation. Mech. Dev. 122, 573-585.
11. Brent, A. E. and Tabin, C. J. (2002). Developmental regulation of somite derivatives: muscle, cartilage and tendon. Curr. Opin. Genet. Dev. 12, 548-557.
12. Brent, A. E. and 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, 3885-3896.
13. Brent, A. E., Schweitzer, R. and Tabin, C. J. (2003). A somitic compartment of tendon progenitors. Cell 113, 235-248.
14. Brent, A. E., Braun, T. and Tabin, C. J. (2005). Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development. Development 132, 515-528. (Pubitemid 40277692)
15. Brown, N. H. (2000). Cell-cell adhesion via the ECM: integrin genetics in fly and worm. Matrix Biol. 19, 191-201.
16. Callahan, C. A., Bonkovsky, J. L., Scully, A. L. and Thomas, J. B. (1996). derailed is required for muscle attachment site selection in Drosophila. Development 122, 2761-2767.
17. Chai, Y., Jiang, X., Ito, Y., Bringas, P., Jr, Han, J., Rowitch, D. H., Soriano, P., McMahon, A. P. and Sucov, H. M. (2000). Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127, 1671-1679.
18. Chanana, B., Graf, R., Koledachkina, T., Pflanz, R. and Vorbruggen, G. (2007). AlphaPS2 integrin-mediated muscle attachment in Drosophila requires the ECM protein Thrombospondin. Mech. Dev. 124, 463-475.
19. Chanana, B., Steigemann, P., Jackle, H. and Vorbruggen, G. (2009). Reception of Slit requires only the chondroitin-sulphate-modified extracellular domain of Syndecan at the target cell surface. Proc. Natl. Acad. Sci. USA 106, 11984-11988.
20. Conti, F. J., Felder, A., Monkley, S., Schwander, M., Wood, M. R., Lieber, R., Critchley, D. and Muller, U. (2008). Progressive myopathy and defects in the maintenance of myotendinous junctions in mice that lack talin 1 in skeletal muscle. Development 135, 2043-2053.
21. Conti, F. J., Monkley, S. J., Wood, M. R., Critchley, D. R. and Muller, U. (2009). Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junctions. Development 136, 3597-3606.
22. Couly, G. F., Coltey, P. M. and Le Douarin, N. M. (1992). The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114, 1-15.
23. Cserjesi, P., Brown, D., Ligon, K. L., Lyons, G. E., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Olson, E. N. (1995). Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 121, 1099-1110.
24. della Gaspera, B., Armand, A. S., Sequeira, I., Lecolle, S., Gallien, C. L., Charbonnier, F. and Chanoine, C. (2009). The Xenopus MEF2 gene family: evidence of a role for XMEF2C in larval tendon development. Dev. Biol. 328, 392-402.
25. Edom-Vovard, F. and Duprez, D. (2004). Signals regulating tendon formation during chick embryonic development. Dev. Dyn. 229, 449-457.
26. Edom-Vovard, F., Bonnin, M. and Duprez, D. (2001). Fgf8 transcripts are located in tendons during embryonic chick limb development. Mech. Dev. 108, 203-206. (Pubitemid 32918191)
27. Edom-Vovard, F., Schuler, B., Bonnin, M. A., Teillet, M. A. and Duprez, D. (2002). Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Dev. Biol. 247, 351-366.
28. Eloy-Trinquet, S., Wang, H., Edom-Vovard, F. and Duprez, D. (2009). Fgf signaling components are associated with muscles and tendons during limb development. Dev. Dyn. 238, 1195-1206.
29. Espira, L., Lamoureux, L., Jones, S. C., Gerard, R. D., Dixon, I. M. and Czubryt, M. P. (2009). The basic helix-loop-helix transcription factor scleraxis regulates fibroblast collagen synthesis. J. Mol. Cell. Cardiol. 47, 188-195.
30. Estrada, B., Gisselbrecht, S. S. and Michelson, A. M. (2007). The transmembrane protein Perdido interacts with Grip and integrins to mediate myotube projection and attachment in the Drosophila embryo. Development 134, 4469-4478.
31. Fernandes, J. J., Celniker, S. E. and VijayRaghavan, K. (1996). Development of the indirect flight muscle attachment sites in Drosophila: role of the PS integrins and the stripe gene. Dev. Biol. 176, 166-184.
32. Fogerty, F. J., Fessler, L. I., Bunch, T. A., Yaron, Y., Parker, C. G., Nelson, R. E., Brower, D. L., Gullberg, D. and Fessler, J. H. (1994). Tiggrin, a novel Drosophila extracellular matrix protein that functions as a ligand for Drosophila alpha PS2 beta PS integrins. Development 120, 1747-1758.
33. Frommer, G., Vorbruggen, G., Pasca, G., Jackle, H. and Volk, T. (1996). Epidermal egr-like zinc finger protein of Drosophila participates in myotube guidance. EMBO J. 15, 1642-1649.
34. Fukuta, S., Oyama, M., Kavalkovich, K., Fu, F. H. and Niyibizi, C. (1998). Identification of type II, IX and X collagens at the insertion site of the bovine achilles tendon. Matrix Biol. 17, 65-73. (Pubitemid 28206024)
35. Gilsohn, E. and Volk, T. (2010a). Slowdown promotes muscle integrity by modulating integrin-mediated adhesion at the myotendinous junction. Development 137, 785-794.
36. Gilsohn, E. and Volk, T. (2010b). A screen for tendon-specific genes uncovers new and old components involved in muscle-tendon interaction. Fly (Austin) 4, 149-153.
37. Gotwals, P. J., Fessler, L. I., Wehrli, M. and Hynes, R. O. (1994). Drosophila PS1 integrin is a laminin receptor and differs in ligand specificity from PS2. Proc. Natl. Acad. Sci. USA 91, 11447-11451.
38. Grenier, J., Teillet, M. A., Grifone, R., Kelly, R. G. and Duprez, D. (2009). Relationship between neural crest cells and cranial mesoderm during head muscle development. PLoS ONE 4, e4381.
39. Grifone, R., Jarry, T., Dandonneau, M., Grenier, J., Duprez, D. and Kelly, R. G. (2008). Properties of branchiomeric and somite-derived muscle development in Tbx1 mutant embryos. Dev. Dyn. 237, 3071-3078.
40. Hall, B. K. and Herring, S. W. (1990). Paralysis and growth of the musculoskeletal system in the embryonic chick. J. Morphol. 206, 45-56.
41. Hamburger, V. (1939). The development and innervation of transplanted limb primordia of chick embryos. J. Exp. Zool. 80, 347-389.
42. Hamburger, V. (1940). The primary development of the skeleton in nerveless and poorly innervated limb transplants of chick embryos. Physiol. Zool. 13, 367-384.
43. Hatini, V. and DiNardo, S. (2001). Divide and conquer: pattern formation in Drosophila embryonic epidermis. Trends Genet. 17, 574-579.
44. Hosseini, A. and Hogg, D. A. (1991). The effects of paralysis on skeletal development in the chick embryo. II. Effects on histogenesis of the tibia. J. Anat. 177, 169-178.
45. Hurle, J. M., Ros, M. A., Ganan, Y., Macias, D., Critchlow, M. and Hinchliffe, J. R. (1990). Experimental analysis of the role of ECM in the patterning of the distal tendons of the developing limb bud. Cell Differ. Dev. 30, 97-108.
46. Kablar, B. and Rudnicki, M. A. (2000). Skeletal muscle development in the mouse embryo. Histol. Histopathol. 15, 649-656.
47. Kardon, G. (1998). Muscle and tendon morphogenesis in the avian hind limb. Development 125, 4019-4032.
48. Kieny, M. and Chevallier, A. (1979). Autonomy of tendon development in the embryonic chick wing. J. Embryol. Exp. Morphol. 49, 153-165.
49. Kontges, G. and Lumsden, A. (1996). Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122, 3229-3242.
50. Kramer, S. G., Kidd, T., Simpson, J. H. and Goodman, C. S. (2001). Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 292, 737-740. (Pubitemid 32385546)
51. Kronenberg, H. M. (2003). Developmental regulation of the growth plate. Nature 423, 332-336.
52. Kumagai, J., Sarkar, K., Uhthoff, H. K., Okawara, Y. and Ooshima, A. (1994). Immunohistochemical distribution of type I, II and III collagens in the rabbit supraspinatus tendon insertion. J. Anat. 185, 279-284.
53. Lejard, V., Brideau, G., Blais, F., Salingcarnboriboon, R., Wagner, G., Roehrl, M. H., Noda, M., Duprez, D., Houillier, P. and Rossert, J. (2007). Scleraxis and NFATc regulate the expression of the pro-alpha1(I) collagen gene in tendon fibroblasts. J. Biol. Chem. 282, 17665-17675.
54. Logan, M., Martin, J. F., Nagy, A., Lobe, C., Olson, E. N. and Tabin, C. J. (2002). Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80.
55. Lorda-Diez, C. I., Montero, J. A., Martinez-Cue, C., Garcia-Porrero, J. A. and Hurle, J. M. (2009). Transforming growth factors beta coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J. Biol. Chem. 284, 29988-29996.
56. Martin, D., Zusman, S., Li, X., Williams, E. L., Khare, N., DaRocha, S., Chiquet-Ehrismann, R. and Baumgartner, S. (1999). wing blister, a new Drosophila laminin alpha chain required for cell adhesion and migration during embryonic and imaginal development. J. Cell Biol. 145, 191-201.
57. Murchison, N. D., Price, B. A., Conner, D. A., Keene, D. R., Olson, E. N., Tabin, C. J. and Schweitzer, R. (2007). Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 134, 2697-2708.
58. Nabel-Rosen, H., Dorevitch, N., Reuveny, A. and Volk, T. (1999). The balance between two isoforms of the Drosophila RNA-binding protein how controls tendon cell differentiation. Mol. Cell 4, 573-584. (Pubitemid 29531137)
59. Nabel-Rosen, H., Volohonsky, G., Reuveny, A., Zaidel-Bar, R. and Volk, T. (2002). Two isoforms of the Drosophila RNA binding protein, how, act in opposing directions to regulate tendon cell differentiation. Dev. Cell 2, 183-193.
60. Oka, K., Oka, S., Hosokawa, R., Bringas, P., Jr, Brockhoff, H. C., 2nd, Nonaka, K. and Chai, Y. (2008). TGF-beta mediated Dlx5 signaling plays a crucial role in osteo-chondroprogenitor cell lineage determination during mandible development. Dev. Biol. 321, 303-309.
61. Olsen, B. R., Reginato, A. M. and Wang, W. (2000). Bone development. Annu. Rev. Cell Dev. Biol. 16, 191-220.
62. Pai, A. C. (1965). Developmental genetics of a lethal mutation, muscular dysgenesis (Mdg), in the mouse. Ii. Developmental analysis. Dev. Biol. 11, 93-109.
63. Piepenburg, O., Vorbruggen, G. and Jackle, H. (2000). Drosophila segment borders result from unilateral repression of hedgehog activity by wingless signaling. Mol. Cell 6, 203-209.
64. Pownall, M. E., Gustafsson, M. K. and Emerson, C. P., Jr (2002). Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747-783.
65. Pryce, B. A., Watson, S. S., Murchison, N. D., Staverosky, J. A., Dunker, N. and Schweitzer, R. (2009). Recruitment and maintenance of tendon progenitors by TGF{beta} signaling are essential for tendon formation. Development 136, 1351-1361.
66. Ralphs, J. R., Benjamin, M., Waggett, A. D., Russell, D. C., Messner, K. and Gao, J. (1998). Regional differences in cell shape and gap junction expression in rat Achilles tendon: relation to fibrocartilage differentiation. J. Anat. 193, 215-222.
67. -/- amyogenic fetuses reveal the importance of early contraction and static loading by striated muscle in mouse skeletogenesis. Dev. Genes Evol. 216, 1-9.
68. Schnorrer, F. and Dickson, B. J. (2004). Muscle building; mechanisms of myotube guidance and attachment site selection. Dev. Cell 7, 9-20.
69. Schnorrer, F., Kalchhauser, I. and Dickson, B. J. (2007). The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev. Cell 12, 751-766.
70. Schweitzer, R., Chyung, J. H., Murtaugh, L. C., Brent, A. E., Rosen, V., Olson, E. N., Lassar, A. and Tabin, C. J. (2001). Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments. Development 128, 3855-3866.
71. Shellswell, G. B. and Wolpert, L. (1977). The pattern of muscle and tendon development in the chick wing. In Vertebrate Limb and Somite Morphogenesis (ed. D. A. Ede, J. R. Hincliffe and M. Balls), pp. 71-86. Cambridge, UK: Cambridge University Press.
72. Shukunami, C., Takimoto, A., Oro, M. and Hiraki, Y. (2006). Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev. Biol. 298, 234-247.
73. Smith, T. G., Sweetman, D., Patterson, M., Keyse, S. M. and Munsterberg, A. (2005). Feedback interactions between MKP3 and ERK MAP kinase control scleraxis expression and the specification of rib progenitors in the developing chick somite. Development 132, 1305-1314.
74. Subramanian, A., Wayburn, B., Bunch, T. and Volk, T. (2007). Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development 134, 1269-1278.
75. Swan, L. E., Wichmann, C., Prange, U., Schmid, A., Schmidt, M., Schwarz, T., Ponimaskin, E., Madeo, F., Vorbruggen, G. and Sigrist, S. J. (2004). A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev. 18, 223-237.
76. Swan, L. E., Schmidt, M., Schwarz, T., Ponimaskin, E., Prange, U., Boeckers, T., Thomas, U. and Sigrist, S. J. (2006). Complex interaction of Drosophila GRIP PDZ domains and Echinoid during muscle morphogenesis. EMBO J. 25, 3640-3651.
77. Tanentzapf, G. and Brown, N. H. (2006). An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton. Nat. Cell Biol. 8, 601-606.
78. Thomopoulos, S., Williams, G. R., Gimbel, J. A., Favata, M. and Soslowsky, L. J. (2003). Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. J. Orthop. Res. 21, 413-419. (Pubitemid 36546807)
79. Towers, M. and Tickle, C. (2009). Growing models of vertebrate limb development. Development 136, 179-190.
80. Tozer, S. and Duprez, D. (2005). Tendon and ligament: development, repair and disease. Birth Defects Res. C Embryo Today 75, 226-236.
81. Trainor, P. A., Tan, S. S. and Tam, P. P. (1994). Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development 120, 2397-2408.
82. Tremblay, P., Dietrich, S., Mericskay, M., Schubert, F. R., Li, Z. and Paulin, D. (1998). A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Dev. Biol. 203, 49-61.
83. Usui, K., Pistillo, D. and Simpson, P. (2004). Mutual exclusion of sensory bristles and tendons on the notum of dipteran flies. Curr. Biol. 14, 1047-1055.
84. Volk, T. (1999). Singling out Drosophila tendon cells: a dialogue between two distinct cell types. Trends Genet. 15, 448-453.
85. Volk, T. and VijayRaghavan, K. (1994). A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 120, 59-70.
86. Volohonsky, G., Edenfeld, G., Klambt, C. and Volk, T. (2007). Muscle-dependent maturation of tendon cells is induced by post-transcriptional regulation of stripeA. Development 134, 347-356.
87. Wayburn, B. and Volk, T. (2009). LRT, a tendon-specific leucine-rich repeat protein, promotes muscle-tendon targeting through its interaction with Robo. Development 136, 3607-3615.
88. Yarnitzky, T., Min, L. and Volk, T. (1997). The Drosophila neuregulin homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes Dev. 11, 2691-2700. (Pubitemid 27452392)
89. Yoon, Y. S., Lee, J. H., Hwang, S. C., Choi, K. S. and Yoon, G. (2005). TGF beta1 induces prolonged mitochondrial ROS generation through decreased complex IV activity with senescent arrest in Mv1Lu cells. Oncogene 24, 1895-1903.
90. Ypsilanti, A. R., Zagar, Y. and Chedotal, A. (2010). Moving away from the midline: new developments for Slit and Robo. Development 137, 1939-1952.