Skip to main content

Advertisement

Log in

Extraocular Muscle Repair and Regeneration

  • Regenerative Medicine in Ophthalmology (D Myung, Section Editor)
  • Published:
Current Ophthalmology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The goal of this review is to summarize the unique regenerative milieu within mature mammalian extraocular muscles (EOMs). This will aid in understanding disease propensity for and sparing of EOMs in skeletal muscle diseases as well as the recalcitrance of the EOM to injury.

Recent Findings

The EOMs continually remodel throughout life and contain an extremely enriched number of myogenic precursor cells that differ in number and functional characteristics from those in limb skeletal muscle. The EOMs also contain a large population of Pitx2-positive myogenic precursor cells that provide the EOMs with many of their unusual biological characteristics, such as myofiber remodeling and skeletal muscle disease sparing. This environment provides for rapid and efficient remodeling and regeneration after various types of injury. In addition, the EOMs show a remarkable ability to respond to perturbations of single muscles with coordinated changes in the other EOMs that move in the same plane.

Summary

These data will inform ophthalmologists as they work toward developing new treatments for eye movement disorders, new approaches for repair after nerve or direct EOM injury, as well as suggest potential explanations for the unusual disease propensity and disease-sparing characteristics of human EOM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Van Campenhout A, Molenaers G. Localization of the motor endplate zone in human skeletal muscles of the lower limb: anatomical guidelines for injection with botulinum toxin. Dev Med Child Neurol. 2011;53:108–19.

    Article  PubMed  Google Scholar 

  2. Chow RS, Medri MK, Martin DC, Leekam RN, Agur AM, McKee NH. Sonographic studies of human soleus and gastrocnemius muscle architecture: gender variability. Eur J Appl Physiol. 2000;82:236–44.

    Article  CAS  PubMed  Google Scholar 

  3. Gauthier GF, Lowey S. Distribution of myosin isoenzymes among skeletal muscle fiber types. J Cell Biol. 1979;81:10–25.

    Article  CAS  PubMed  Google Scholar 

  4. McLoon LK, Willoughby CL, Andrade FH. Extraocular muscles: structure and function. In: Craniofacial muscles: a new framework for understanding the effector side of craniofacial muscles. Eds: LK McLoon, F Andrade. Springer, 2012; Chapter 3; pp. 31–88.

  5. Kupfer C. Motor innervation of extraocular muscle. J Physiol. 1960;153:522–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jacoby J, Chiarandini DJ, Stefani E. Electrical properties and innervation of fibers in the orbital layer of rat extraocular muscles. J Neurophysiol. 1989;61:116–25.

    CAS  PubMed  Google Scholar 

  7. Davidowitz J, Philips G, Breinin GM. Organization of the orbital surface layer in rabbit superior rectus. Invest Ophthalmol Vis Sci. 1977;16:711–29.

    CAS  PubMed  Google Scholar 

  8. McLoon LK, Rios L, Wirtschafter JD. Complex three-dimensional patterns of myosin isoform expression: differences between and within specific extraocular muscles. J Muscle Res Cell Motil. 1999;20:771–83.

    Article  CAS  PubMed  Google Scholar 

  9. Wieczorek DF, Periasamy M, Butler-Browne GS, Whalen RG, Nadal-Ginard B. Co-expression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular musculature. J Cell Biol. 1985;10:618–29.

    Article  Google Scholar 

  10. McLoon LK, Park H, Kim JH, Pedrosa-Domellöf F, Thompson LV. A continuum of myofibers in adult rabbit extraocular muscle: force, shortening velocity, and patterns of myosin heavy chain co-localization. J Appl Physiol. 2011;111:1178–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Close RI, Ar L. Dynamic properties of inferior rectus muscle of the rat. J Physiol. 1974;236:259–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fuchs AF, Binder MD. Fatigue resistance of human extraocular muscles. J Neurophysiol. 1988;60:1874–95.

    CAS  PubMed  Google Scholar 

  13. Porter JD, Khanna S, Kaminski HJ, Rao JS, Merriam AP, Richmonds CR, Leahy P, Li J, Andrade FH. Extraocular muscle is defined by a fundamentally distinct gene expression profile. Proc Natl Acad Sci USA. 2001;98:12062–7.

  14. Fraterman S, Zeiger U, Khurana TS, Rubinstein NA, Wilm M. Combination of OFFGEL fractionation and label-free quantitation facilitated proteomics of extraocular muscle. Proteomics. 2007;7:3404–16.

    Article  CAS  PubMed  Google Scholar 

  15. Tajbakhsh S, Rocancout D, Cossu G, Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and myf-5 act upstream of MyoD. Cell. 1997;89:127–38.

    Article  CAS  PubMed  Google Scholar 

  16. Diehl AG, Zareparsi S, Qian M, Khanna R, Angeles R, Gage PJ. Extraocular muscle morphogenesis and gene expression are regulated by Pitx2 gene dose. Invest Ophthalmol Vis Sci. 2006;47:1785–93.

    Article  PubMed  Google Scholar 

  17. Zhou Y, Cheng G, Dieter L, Hjalt TA, Andrade FH, Stahl JS, Kaminski HJ. An altered phenotype in a conditional knockout of Pitx2 in extraocular muscle. Invest Ophthalmol Vis Sci. 2009;50:4531–41.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zhou Y, Liu D, Kaminski HJ. Pitx2 regulates myosin heavy chain isoform expression and multi-innervation in extraocular muscle. J Physiol. 2011;589:4601–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–5.

  20. Seale P, Sabourin LA, Girgis-Garbardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000;102:777–86.

    Article  CAS  PubMed  Google Scholar 

  21. •• Keefe AC, Lawson JA, Flygare SD, Fox ZD, Colasanto MP, Mathew SJ, Yandell M, Kardon G. Muscle stem cells contribute to myofibers in sedentary adult mice. Nat Commun. 2015;6:7087. Pax7 lineage tracing in adult skeletal muscles

  22. •• Pawlikowski B, Pulliam C, Betta ND, Kardon G, Olwin B. Pervasive satellite cell contribution to uninjured adult muscle fibers. Skelet Muscle. 2015;5:42. doi:10.1186/s13395-015-0067. Pax7 lineage tracing in adult skeletal muscles

  23. McLoon LK, Wirtschafter JD. Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci. 2003;44:1927–32.

    Article  PubMed  PubMed Central  Google Scholar 

  24. • McDonald AA, Kunz MD, McLoon LK. Dystrophic changes in extraocular muscles after gamma irradiation in mdx:utrophin(+/−) mice. PLoS One. 2014;9(1):e86424. Demonstration of a radiation resistant myogenic precursor cell in extraocular muscle.

  25. • Kallestad KM, Hebert SL, McDonald AA, Daniel ML, Cu SR, McLoon LK. Sparing of the extraocular muscle in aging and muscular dystrophies: a myogenic precursor cell hypothesis. Exp Cell Res. 2011;317:873–5. Study demonstrating an enriched population of muscle precursor cells in extraocular muscle in the mdx mouse

  26. Lindström M, Tjust AE, PedrosaDomellöf F. Pax7-positive cells/satellite cells in human extraocular muscles. Invest Ophthalmol Vis Sci. 2015;56:6132–43.

    Article  PubMed  Google Scholar 

  27. Stuelsatz P, Shearer A, Li Y, Muir LA, Ieronimakis N, Shen QW, Kirillova I, Yablonka-Reuveni Z. Extraocular muscle satellite cells are high performance myo-engines retaining efficient regeneration capacity in dystrophin deficiency. Dev Biol. 2015;397:31–44.

    Article  CAS  PubMed  Google Scholar 

  28. • Nogueira JM, Hawrot K, Sharpe C, Noble A, Wood WM, Jorge EC, Goldhamer DJ, Kardon G, Dietrich S. The emergence of Pax7-expressing muscle stem cells during vertebrate head muscle development. Front Aging Neurosci. 2015;7:62. Study showing that Pax7 is not expressed early in cranial muscle development

  29. Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA. Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol. 2006;172:103–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. •• Hebert SL, Daniel ML, McLoon LK. The role of Pitx2 in maintaining the phenotype of myogenic precursor cells in the extraocular muscles. PLoS One. 2013;8(3):e58405. Study showing Pitx2-positive myogenic precursor cells in the extraocular muscles

  31. Gage PJ, Zacharias AL. Signaling “cross-talk” is integrated by transcription factors in the development of the anterior segment of the eye. Dev Dyn. 2009;238:2149–62.

  32. Shih HP, Gross MK, Kioussi C. Muscle development: forming the head and trunk muscles. Acta Histochem. 2008;110:97–108.

  33. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA. Myogenic specification of side population cells in skeletal muscle. J Cell Biol. 2002;159:123–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Pacheco-Pinedo EC, Budak MT, Zeiger U, Jorgensen LH, Bogdanovich S, Schroder HD, Rubinstein NA, Khurana TS. Transcriptional and functional differences in stem cell populations isolated from extraocular and limb muscles. Physiol Genomics. 2009;37:35–42.

    Article  CAS  PubMed  Google Scholar 

  35. Bildsoe H, Loebel DA, Jones VJ, Hor AC, Braithwaite AW, Chen YT, Behringer RR, Tam PP. The mesenchymal architecture of the cranial mesoderm of mouse embryos is disrupted by the loss of Twist1 function. Dev Biol. 2013;374:295–307.

    Article  CAS  PubMed  Google Scholar 

  36. Vincentz JW, Barnes RM, Rodgers R, Firulli BA, Conway SJ, Firulli AB. An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev Biol. 2008;320:131–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Matt N, Ghyselinck NB, Pellerin I, Dupe V. Impairing retinoic acid signaling in the neural crest cells is sufficient to alter entire eye morphogenesis. Dev Biol. 2008;320:1401–48.

    Article  Google Scholar 

  38. •• Bohnsack BL, Gallina D, Thompson H, Kasprick DS, Lucarellie MJ, Dootz G, Nelson C, McGonnell IM, Kahana A. Development of extraocular muscles requires early signals from periocular neural crest and the developing eye. Arch Ophthalmol. 2011;129:1030–41. Study showing that neural crest cells control early extraocular muscle development

  39. Liu N, Garry GA, Li S, Bezprozvannava S, Sanchez-Ortiz E, Chen B, Shelton JM, Jaichander P, Dabbel-Duby R, Olson EN. A Twist2-dependent progenitor cell contributes to adult skeletal muscle. Nat Cell Biol. 2017;19:202–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. •• Formicola L, Marazzi G, Sassoon DA. The extraocular muscle stem cell niche is resistant to ageing and disease. Front Aging Neurosci. 2014;6:328. Study of the unique properties of the stem cell niche in extraocular muscles

  41. • Saera-Vila A, Kasprick DS, Junttila TL, Grzegorski SJ, Louie KW, Chiaria EF, Kish PE, Kahana A. Myocyte dedifferentiation derives extraocular muscle regeneration in adult zebrafish. Invest Ophthalmol Vis Sci. 2015;56:4977–93. Study of the processes used for regeneration of extraocular muscle in zebrafish

  42. Govindan M, Mohney BG, Diehl NN, Burke JP. Incidence and types of childhood exotropia: a population-based study. Ophthalmology. 2005;112:104–8.

    Article  PubMed  Google Scholar 

  43. Greenberg AR, Mohney BG, Diehl NN, Burke JP. Incidence and types of childhood esotropia: a population-based study. Ophthalmology. 2007;114:170–4.

    Article  PubMed  Google Scholar 

  44. Ludwig IH. Scar remodeling after strabismus surgery. Trans Am Ophthalmol Soc. 1999;97:583–651.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Tinley C, Evans S, McGrane D, Quinn A. Single medial rectus muscle advancement in stretched scar consecutive exotropia. J AAPOS. 2010;14:120–3.

    Article  PubMed  Google Scholar 

  46. Nelson LB, Ervin-Mulvey LD, Calhoun JH, Harley RD, Keisler MS. Surgical management for abnormal head posture in nystagmus: the augmented modified Kestenbaum procedure. Brit J Ophthalmol. 1984;68:796–800.

    Article  CAS  Google Scholar 

  47. Vroman DT, Hutchinson AK, Saunders RA, Wilson ME. Two-muscle surgery for congenital esotropia: rate of reoperation in patients with small versus large angles of deviation. J AAPOS. 2000;4:267–70.

    Article  CAS  PubMed  Google Scholar 

  48. • Pineles SL, Ela-Dalman N, Zvansky AG, Yu F, Rosenbaum AL. Long-term results of the surgical management of intermittent exotropia. J AAPOS. 2010;14:298–304. Examination of the efficacy of surgical management of strabismus

  49. Livir-Rallatos G, Gunton KB, Calhoun JH. Surgical results for large-angle exotropia. J AAPOS. 2002;6:77–80.

    Article  PubMed  Google Scholar 

  50. Christiansen SP, Soulsby ME, Seifen EE. Effect of antagonist weakening on developed tension in cat extraocular muscle. Invest Ophthalmol Vis Sci. 1995;36:2547–50.

    CAS  PubMed  Google Scholar 

  51. Christiansen SP, Madhat M, Baker L, Baker R. Fiber hypertrophy in rat extraocular muscle following lateral rectus resection. J Pedatri Ophthalmol Strabismus. 1988;25:167–71.

  52. Christiansen SP, McLoon LK. The effect of resection on satellite cell activity in rabbit extraocular muscle. Invest Ophthalmol Vis Sci. 2006;47:605–13.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Christiansen SP, Antunes-Forschini RS, McLoon LK. Effects of recession versus tenotomy surgery without recession in adult rabbit extraocular muscle. Invest Ophthalmol Vis Sci. 2010;51:5646–56.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Shin SY, Park DJ. Expression of four growth factors in recessed extraocular muscles of rabbits. Ophthalmic Surg Lasers Imaging. 2006;37:129–37.

    PubMed  Google Scholar 

  55. • Wang L, Nelson LB. One muscle strabismus surgery. Curr Opin Ophthalmol. 2010;21:335–40. Examination of the efficacy of one muscle surgical treatment of strabismus

  56. Brin MR. Botulinum toxin: chemistry, pharmacology, toxicity, and immunology. Muscle Nerve Suppl. 1997;6:S61–91.

    Google Scholar 

  57. Hassan SM, Jennekens FGI, Veldman H. Botulinum toxin-induced myopathy in the rat. Brain. 1995;118:533–45.

    Article  PubMed  Google Scholar 

  58. Pinter MJ, Van den Noven S, Muccio D, Wallace N. Axotomy-like changes in cat motoneuron electrical properties elicited by botulinum toxin depend on the complete elimination of neuromuscular transmission. J Neurosci. 1991;11:657–66.

    CAS  PubMed  Google Scholar 

  59. Porter JD, Strebeck S, Capra NF. Botulinum-induced changes in monkey eyelid muscle. Comparison with changes seen in extraocular muscle. Arch Ophthalmol. 1991;109:396–404.

    Article  CAS  PubMed  Google Scholar 

  60. Spencer RF, McNeer KW. Botulinum toxin paralysis of adult monkey extraocular muscle: structural alterations in orbital, singly innervated muscle fibers. Arch Ophthalmol. 1987;105:1703–11.

    Article  CAS  PubMed  Google Scholar 

  61. Krancj BS, Sketelj J, D’Albis A, Erzen I. Long-term changes in myosin heavy chain composition after botulinum toxin a injection into rat medial rectus muscle. Invest Ophthalmol Vis Sci. 2001;42:3158–64.

    Google Scholar 

  62. Croes SA, Baryshnikova LM, Kaluskar SS, von Bartheld CS. Acute and long-term effects of botulinum neurotoxin on the function and structure of developing extraocular muscles. Neurobiol Dis. 2007;25:649–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ugalde I, Christiansen SP, McLoon LK. Botulinum toxin treatment of extraocular muscles in rabbits results in increased myofiber remodeling. Invest Ophthalmol Vis Sci. 2005;46:4114–20.

    Article  PubMed  PubMed Central  Google Scholar 

  64. • Liu W, Wei-LaPierre L, Klose A, Dirksen RT, Chakkalakal JV. Inducible depletion of adult skeletal muscle stem cells impairs the regeneration of neuromuscular junctions. elife. 2015;27:4. doi:10.7554/eLife.09221. Demonstration that myogenic precursor cells are critical for the regeneration of neuromuscular junctions after injury

  65. Foster AH, Carlson BM. Myotoxicity of local anesthetics and regeneration of the damaged muscle fibers. AnesthAnalg. 1980;59:727–36.

    CAS  Google Scholar 

  66. Rainin EA, Carlson BM. Postoperative diplopia and ptosis. A clinical hypothesis based on the myotoxicity of local anesthetics. Arch Ophthalmol. 1985;103:1337–9.

    Article  CAS  PubMed  Google Scholar 

  67. Guyton DL. Strabismic complications from local anesthetics. Semin Ophthalmol. 2008;23:298–301.

  68. Carlson BM, Emerick S, Komorowski TE, Rainin EA, Shepard BM. Extraocular muscle regeneration in primates. Local anesthetic induced lesions. Ophthalmology. 1992;99:582–9.

    Article  CAS  PubMed  Google Scholar 

  69. Zhang C, Phamonvaechavan P, Rajan A, Poon DY, Topcu-Yilmaz P, Guyton D. Concentration-dependent bupivacaine myotoxicity in rabbit extraocular muscle. J AAPOS. 2010;14:323–7.

    Article  PubMed  Google Scholar 

  70. Porter JD, Edney DP, McMahon EJ, Burns LA. Extraocularmyotoxicity of the retrobulbar anesthetic bupivacaine hydrochloride. Invest Ophthalmol Vis Sci. 1988;29:163–74.

    CAS  PubMed  Google Scholar 

  71. Irving EL, Arshinoff SA, Samis W, Lillakas L, Lui B, Laporte JT, Steinbach MJ. Effect of retrobulbar injection of lidocaine on saccadic velocities. J Cataract Refract Surg. 2004;30:350–6.

    Article  PubMed  Google Scholar 

  72. Scott AB, Miller JM, Shieh KR. Treating strabismus by injecting the agonist muscle with bupivacaine and the antagonist with botulinum toxin. Trans Am Ophthalmol Soc. 2009;107:104–9.

    PubMed  PubMed Central  Google Scholar 

  73. Karpati G, Carpenter S. Small-caliber skeletal muscle fibers do not suffer deleterious consequences of dystrophic gene expression. Am J Med Genet. 1986;25:653–8.

    Article  CAS  PubMed  Google Scholar 

  74. Andrade FH, Porter JD, Kaminski HJ. Eye muscle sparing by the muscular dystrophies: lessons to be learned? Microsc Res Tech. 2000;48:192–203.

    Article  CAS  PubMed  Google Scholar 

  75. • Benítez-Temiño B, Davis-López de Carrizosa MA, Morcuende SR, Matarredona ER, de la Cruz RR, Pastor AM. Functional diversity of neurotrophin actions on the oculomotor system. Int J Molec Sci. 2016;17:pii.E2016. Review of the role played by neurotrophic factors in the function of the ocular motor system

  76. McLoon LK, Christiansen SP. Increasing extraocular muscle strength with insulin-like growth factor II. Invest Ophthalmol Vis Sci. 2003;44:3866–72.

    Article  PubMed  Google Scholar 

  77. Feng C, von Bartheld CS. Expression of insulin-like growth factor 1 isoforms in the rabbit oculomotor system. Growth Hormon IGF Res. 2011;21:228–32.

    Article  CAS  Google Scholar 

  78. Davis-López de Carrizosa MA, Morado-Díaz CJ, Tena JJ, Benítez-Temiño B, Pecero ML, Morcuende SR, de la Cruz RR, Pastor AM. Complementary actions of BDNF and neurotrophin-3 on the firing patterns and synaptic composition of motoneurons. J Neurosci. 2009;29:575–87.

    Article  PubMed  Google Scholar 

  79. • Willoughby CL, Fleuriet J, Walton MM, Mustari MJ, McLoon LK. Adaptation of slow myofibers: the effect of sustained BDNF treatment of extraocular muscles in infant nonhuman primates. Invest Ophthalmol Vis Sci. 2015;56:3467–83. Study looking at the effect of exogenous treatment with brain derived neurotrophic factor on the infant monkey extraocular muscle

  80. • Agarwal AB, Feng CY, Altick AL, Quilici DR, Wen D, Johnson LA, von Bartheld CS. Altered protein composition and gene expression in strabismic human extraocular muscles and tendons. Invest Ophthalmol Vis Sci. 2016;57:5576–85. Analysis of genes that are down- or up-regulated in muscles from strabismic subjects

  81. • Harandi VM, Lindquist S, Kolan SS, Brännström T, Liu JX. Analysis of neurotrophic factors in limb and extraocular muscles of mouse model of amyotrophic lateral sclerosis. PLoS One. 2014;9(10):e109833. Demonstration of the role of neurotrophic factors in the differential effects of amyotrophic lateral sclerosis on extraocular and limb muscles

  82. Steljes TP, Kinoshita Y, Wheeler EF, Oppenheim RW, von Bartheld CS. Neurotrophic factor regulation of developing avian oculomotor neurons: differential effects of BDNF and GDNF. J Neurobiol. 1999;41:295–315.

    Article  CAS  PubMed  Google Scholar 

  83. Chen J, von Bartheld CS. Role of exogenous and endogenous trophic factors in the regulation of extraocular muscle strength during development. Invest Ophthalmol Vis Sci. 2004;45:3538–45.

    Article  PubMed  Google Scholar 

  84. Porter JD, Hauser KF. Survival of extraocular muscle in long-term organotypic culture: differential influence of appropriate and inappropriate motoneurons. Dev Biol. 1993;160:39–50.

    Article  CAS  PubMed  Google Scholar 

  85. McLoon LK, Andrade FH. Comparison of craniofacial muscles: a unifying hypothesis. In: Craniofacial muscles: a new framework for understanding the effector side of craniofacial muscles. Eds: LK McLoon, F Andrade. Springer, 2012; Chapter 17. pp. 325–335.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Linda K. McLoon.

Ethics declarations

Conflict of Interest

M.V., K.F., and L.K.M. declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

Animal studies described in this review were performed with approval by the University of Minnesota Animal Care and Use Committee and followed the NIH Animal Care and Use Guidelines.

This work was supported by NIH EY15313 (L.K.M.), NIH RA066454 (M.V.), NIH P30 EY11375, NIH P30AR0507220, Minnesota Lions Foundation, and an unrestricted grant to the Department of Ophthalmology and Visual Sciences from Research to Prevent Blindness, Inc. In addition, this work was supported in part by NIH P30 CA77598 supporting the University Flow Cytometry Resource.

Additional information

This article is part of the Topical Collection on Regenerative Medicine in Ophthalmology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Verma, M., Fitzpatrick, K.R. & McLoon, L.K. Extraocular Muscle Repair and Regeneration. Curr Ophthalmol Rep 5, 207–215 (2017). https://doi.org/10.1007/s40135-017-0141-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40135-017-0141-4

Keywords

Navigation