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Stem Cells International
Volume 2017, Article ID 4276927, 9 pages
https://doi.org/10.1155/2017/4276927
Review Article

Environmental Factors That Influence Stem Cell Migration: An “Electric Field”

1Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, ON, Canada M5S 3E1
2Toronto Rehabilitation Institute, University Health Network, Toronto, ON, Canada M4G 3V9
3Department of Surgery, University of Toronto, Toronto, ON, Canada M5S 3E1

Correspondence should be addressed to Cindi M. Morshead; ac.otnorotu@daehsrom.idnic

Received 26 January 2017; Revised 21 March 2017; Accepted 11 April 2017; Published 15 May 2017

Academic Editor: Alfredo Garcia

Copyright © 2017 Stephanie N. Iwasa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. H. Ussing and K. Zerahn, “Active transport of sodium as the source of electric current in the short-circuited isolated frog skin,” Acta Physiologica Scandinavica, vol. 23, no. 2-3, pp. 110–127, 1951. View at Publisher · View at Google Scholar
  2. M. Chiang, K. R. Robinson, and J. W. Vanable, “Electrical fields in the vicinity of epithelial wounds in the isolated bovine eye,” Experimental Eye Research, vol. 54, no. 6, pp. 999–1003, 1992. View at Publisher · View at Google Scholar · View at Scopus
  3. A. T. Barker, L. F. Jaffe, and J. W. Vanable, “The glabrous epidermis of cavies contains a powerful battery,” American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 242, no. 3, pp. R358–R366, 1982. View at Google Scholar
  4. R. Nuccitelli, P. Nuccitelli, S. Ramlatchan, R. Sanger, and P. J. S. Smith, “Imaging the electric field associated with mouse and human skin wounds,” Wound Repair and Regeneration, vol. 16, no. 3, pp. 432–441, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. M. E. McGinnis and J. W. Vanable, “Electrical fields in Notophthalmus viridescens limb stumps,” Developmental Biology, vol. 116, no. 1, pp. 184–193, 1986. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Chiang, E. J. Cragoe, and J. W. Vanable, “Intrinsic electric fields promote epithelization of wounds in the newt, Notophthalmus viridescens,” Developmental Biology, vol. 146, no. 2, pp. 377–385, 1991. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Zhao, B. Song, J. Pu et al., “Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN,” Nature, vol. 442, no. 7101, pp. 457–460, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Shi and R. B. Borgens, “Three-dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern,” Developmental Dynamics, vol. 202, no. 2, pp. 101–114, 1995. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Shi and R. B. Borgens, “Embryonic neuroepithelial sodium transport, the resulting physiological potential, and cranial development,” Developmental Biology, vol. 165, no. 1, pp. 105–116, 1994. View at Publisher · View at Google Scholar · View at Scopus
  10. K. B. Hotary and K. R. Robinson, “Evidence of a role for endogenous electrical fields in chick embryo development,” Development, vol. 114, no. 4, pp. 985–996, 1992. View at Google Scholar
  11. M. E. M. Metcalf and R. B. Borgens, “Weak applied voltages interfere with amphibian morphogenesis and pattern,” Journal of Experimental Zoology, vol. 268, no. 4, pp. 323–338, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. M. S. Cooper and R. E. Keller, “Perpendicular orientation and directional migration of amphibian neural crest cells in dc electrical fields,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 1, pp. 160–164, 1984. View at Publisher · View at Google Scholar
  13. M. Zhao, A. Agius-Fernandez, J. V. Forrester, and C. D. McCaig, “Directed migration of corneal epithelial sheets in physiological electric fields,” Investigative Ophthalmology & Visual Science, vol. 37, no. 13, pp. 2548–2558, 1996. View at Google Scholar
  14. H. K. Soong, W. C. Parkinson, S. Bafna, G. L. Sulik, and S. C. Huang, “Movements of cultured corneal epithelial cells and stromal fibroblasts in electric fields,” Investigative Ophthalmology & Visual Science, vol. 31, no. 11, pp. 2278–2282, 1990. View at Google Scholar
  15. B. Farboud, R. Nuccitelli, I. R. Schwab, and R. R. Isseroff, “DC electric fields induce rapid directional migration in cultured human corneal epithelial cells,” Experimental Eye Research, vol. 70, no. 5, pp. 667–673, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Wang, M. Zhao, J. V. Forrester, and C. D. McCaig, “Bi-directional migration of lens epithelial cells in a physiological electrical field,” Experimental Eye Research, vol. 76, no. 1, pp. 29–37, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. G. L. Sulik, H. K. Soong, P. C. Chang, W. C. Parkinson, S. G. Elner, and V. M. Elner, “Effects of steady electric fields on human retinal pigment epithelial cell orientation and migration in culture,” Acta Ophthalmologica, vol. 70, no. 1, pp. 115–122, 1992. View at Google Scholar
  18. X. Li and J. Kolega, “Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells,” Journal of Vascular Research, vol. 39, no. 5, pp. 391–404, 2002. View at Publisher · View at Google Scholar
  19. M. J. McKasson, L. Huang, and K. R. Robinson, “Chick embryonic Schwann cells migrate anodally in small electrical fields,” Experimental Neurology, vol. 211, no. 2, pp. 585–587, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Dineur, “Note sur la sensibilité des leucocytes à l’éléctricité,” Bulletin des Séances de la Société Belge de Microscopie (Bruxelles), vol. 18, no. 5, pp. 113–118, 1892. View at Google Scholar
  21. N. Orida and J. D. Feldman, “Directional protrusive pseudopodial activity and motility in macrophages induced by extracellular electric fields,” Cell Motility, vol. 2, no. 3, pp. 243–255, 1982. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Y. Nishimura, R. R. Isseroff, and R. Nuccitelli, “Human keratinocytes migrate to the negative pole in direct current electric fields comparable to those measured in mammalian wounds,” Journal of Cell Science, vol. 109, Part 1, pp. 199–207, 1996. View at Google Scholar
  23. A. I. Chernyavsky, J. Arredondo, E. Karlsson, I. Wessler, and S. A. Grando, “The Ras/Raf-1/MEK1/ERK signaling pathway coupled to integrin expression mediates cholinergic regulation of keratinocyte directional migration,” The Journal of Biological Chemistry, vol. 280, no. 47, pp. 39220–39228, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Ferrier, S. M. Ross, J. Kanehisa, and J. E. Aubin, “Osteoclasts and osteoblasts migrate in opposite directions in response to a constant electrical field,” Journal of Cellular Physiology, vol. 129, no. 3, pp. 283–288, 1986. View at Publisher · View at Google Scholar · View at Scopus
  25. P.-H. G. Chao, R. Roy, R. L. Mauck, W. Liu, W. B. Valhmu, and C. T. Hung, “Chondrocyte translocation response to direct current electric fields,” Journal of Biomechanical Engineering, vol. 122, no. 3, pp. 261–267, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. P.-H. G. Chao, H. H. Lu, C. T. Hung, S. B. Nicoll, and J. C. Bulinski, “Effects of applied DC electric field on ligament fibroblast migration and wound healing,” Connective Tissue Research, vol. 48, no. 4, pp. 188–197, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Babona-Pilipos, I. A. Droujinine, M. R. Popovic, and C. M. Morshead, “Adult subependymal neural precursors, but not differentiated cells, undergo rapid cathodal migration in the presence of direct current electric fields,” PloS One, vol. 6, no. 8, article e23808, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. X. Meng, M. Arocena, J. Penninger, F. H. Gage, M. Zhao, and B. Song, “PI3K mediated electrotaxis of embryonic and adult neural progenitor cells in the presence of growth factors,” Experimental Neurology, vol. 227, no. 1, pp. 210–217, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. T. A. Banks, P. S. B. Luckman, J. E. Frith, and J. J. Cooper-White, “Effects of electric fields on human mesenchymal stem cell behaviour and morphology using a novel multichannel device,” Integrative Biology, vol. 7, no. 6, pp. 693–712, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Zhao, C. Watt, A. Karystinou et al., “Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field,” European Cells & Materials, vol. 22, pp. 344–358, 2011. View at Publisher · View at Google Scholar
  31. J. Zhang, M. Calafiore, Q. Zeng et al., “Electrically guiding migration of human induced pluripotent stem cells,” Stem Cell Reviews, vol. 7, no. 4, pp. 987–996, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. B. A. Reynold and S. Weiss, “Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system,” Science, vol. 255, no. 5052, pp. 1707–1710, 1992. View at Publisher · View at Google Scholar
  33. C. M. Morshead, A. D. Garcia, M. V. Sofroniew, and D. van der Kooy, “The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells,” The European Journal of Neuroscience, vol. 18, no. 1, pp. 76–84, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Cao, D. Wei, B. Reid et al., “Endogenous electric currents might guide rostral migration of neuroblasts,” EMBO Reports, vol. 14, no. 2, pp. 184–190, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. N. M. Branston, A. J. Strong, and L. Symon, “Extracellular potassium activity, evoked potential and tissue blood flow: relationships during progressive ischaemia in baboon cerebral cortex,” Journal of the Neurological Sciences, vol. 32, no. 3, 1977. View at Publisher · View at Google Scholar · View at Scopus
  36. J. A. Hartings, M. L. Rolli, X.-C. M. Lu, and F. C. Tortella, “Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth and neuroprotection,” The Journal of Neuroscience, vol. 23, no. 37, pp. 11602–11610, 2003. View at Google Scholar
  37. A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, and O. Lindvall, “Neuronal replacement from endogenous precursors in the adult brain after stroke,” Nature Medicine, vol. 8, no. 9, pp. 963–970, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Erlandsson, C. H. A. Lin, F. Yu, and C. M. Morshead, “Immunosuppression promotes endogenous neural stem and progenitor cell migration and tissue regeneration after ischemic injury,” Experimental Neurology, vol. 230, no. 1, pp. 48–57, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Faiz, N. Sachewsky, S. Gascón, K. W. A. Bang, C. M. Morshead, and A. Nagy, “Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke,” Cell Stem Cell, vol. 17, no. 5, pp. 624–634, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Marsh and H. W. Beams, “In vitro control of growing chick nerve fibers by applied electric currents,” Journal of Cellular and Comparative Physiology, vol. 27, no. 3, pp. 139–157, 1946. View at Publisher · View at Google Scholar
  41. L. F. Jaffe and M.-M. Poo, “Neurites grow faster towards the cathode than the anode in a steady field,” Journal of Experimental Zoology, vol. 209, no. 1, pp. 115–128, 1979. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Patel and M.-M. Poo, “Orientation of neurite growth by extracellular electric fields,” Journal of Neuroscience, vol. 2, no. 4, pp. 483–496, 1982. View at Google Scholar
  43. Y. Li, X. Wang, and L. Yao, “Directional migration and transcriptional analysis of oligodendrocyte precursors subjected to stimulation of electrical signal,” American Journal of Physiology - Cell Physiology, vol. 309, no. 8, pp. C532–C540, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. M. L. Baer, S. C. Henderson, and R. J. Colello, “Elucidating the role of injury-induced electric fields (EFs) in regulating the astrocytic response to injury in the mammalian central nervous system,” PloS One, vol. 10, no. 11, article e0142740, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Yao, L. Shanley, C. McCaig, and M. Zhao, “Small applied electric fields guide migration of hippocampal neurons,” Journal of Cellular Physiology, vol. 216, no. 2, pp. 527–535, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Yao, A. Pandit, S. Yao, and C. D. McCaig, “Electric field-guided neuron migration: a novel approach in neurogenesis,” Tissue Engineering. Part B, Reviews, vol. 17, no. 3, pp. 143–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Yao and Y. Li, “The role of direct current electric field-guided stem cell migration in neural regeneration,” Stem Cell Reviews and Reports, vol. 12, no. 3, pp. 365–375, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Nakajima, K. Zhu, Y.-H. Sun et al., “KCNJ15/Kir4.2 couples with polyamines to sense weak extracellular electric fields in galvanotaxis,” Nature Communications, vol. 6, p. 8532, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. H.-Y. Yang, R.-P. Charles, E. Hummler, D. L. Baines, and R. R. Isseroff, “The epithelial sodium channel mediates the directionality of galvanotaxis in human keratinocytes,” Journal of Cell Science, vol. 126, Part 9, pp. 1942–1951, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Hanna and M. El-Sibai, “Signaling networks of Rho GTPases in cell motility,” Cellular Signalling, vol. 25, no. 10, pp. 1955–1961, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. E. K. Onuma and S.-W. Hui, “Electric field-directed cell shape changes, displacement, and cytoskeletal reorganization are calcium dependent,” The Journal of Cell Biology, vol. 106, no. 6, pp. 2067–2075, 1988. View at Publisher · View at Google Scholar
  52. H. Zhao, A. Steiger, M. Nohner, and H. Ye, “Specific intensity direct current (DC) electric field improves neural stem cell migration and enhances differentiation towards βIII-tubulin+ neurons,” PloS One, vol. 10, no. 6, article e0129625, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. L. Li, Y. H. El-Hayek, B. Liu et al., “Direct-current electrical field guides neuronal stem/progenitor cell migration,” Stem Cells, vol. 26, no. 8, pp. 2193–2200, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Cao, J. Pu, R. H. Scott, J. Ching, and C. D. McCaig, “Physiological electrical signals promote chain migration of neuroblasts by up-regulating P2Y1 purinergic receptors and enhancing cell adhesion,” Stem Cell Reviews and Reports, vol. 11, no. 1, pp. 75–86, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. M. L. Lalli and A. R. Asthagiri, “Collective migration exhibits greater sensitivity but slower dynamics of alignment to applied electric fields,” Cellular and Molecular Bioengineering, vol. 8, no. 2, pp. 247–257, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. A. R. Tan, E. Alegre-Aguarón, G. D. O’Connell et al., “Passage-dependent relationship between mesenchymal stem cell mobilization and chondrogenic potential,” Osteoarthritis and Cartilage, vol. 23, no. 2, pp. 319–327, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. D. R. Trollinger, R. R. Isseroff, and R. Nuccitelli, “Calcium channel blockers inhibit galvanotaxis in human keratinocytes,” Journal of Cellular Physiology, vol. 193, no. 1, pp. 1–9, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. R. H. W. Funk, “Endogenous electric fields as guiding cue for cell migration,” Frontiers in Physiology, vol. 6, no. 143, pp. 1–8, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. N. Özkucur, T. K. Monsees, S. Perike, H. Q. Do, and R. H. W. Funk, “Local calcium elevation and cell elongation initiate guided motility in electrically stimulated osteoblast-like cells,” PloS One, vol. 4, no. 7, article e6131, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Özkucur, S. Perike, P. Sharma, and R. H. W. Funk, “Persistent directional cell migration requires ion transport proteins as direction sensors and membrane potential differences in order to maintain directedness,” BioMed Central Cell Biology, vol. 12, no. 4, pp. 1–13, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Özkucur, B. Song, S. Bola et al., “NHE3 phosphorylation via PKCη marks the polarity and orientation of directionally migrating cells,” Cellular and Molecular Life Sciences, vol. 71, no. 23, pp. 4653–4663, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Perike, N. Özkucur, P. Sharma et al., “Phospho-NHE3 forms membrane patches and interacts with beta-actin to sense and maintain constant direction during cell migration,” Experimental Cell Research, vol. 324, no. 1, pp. 13–29, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. B. R. Oakley, “Gamma-tubulin: the microtubule organizer?” Trends in Cell Biology, vol. 2, no. 1, pp. 1–5, 1992. View at Publisher · View at Google Scholar
  64. D. Saltukoglu, J. Grünewald, N. Strohmeyer et al., “Spontaneous and electric field-controlled front-rear polarization of human keratinocytes,” Molecular Biology of the Cell, vol. 26, no. 24, pp. 4373–4386, 2015. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Barnes, Y. Shahin, R. Gohil, and I. Chetter, “Electrical stimulation vs. standard care for chronic ulcer healing: a systematic review and meta-analysis of randomised controlled trials,” European Journal of Clinical Investigation, vol. 44, no. 4, pp. 429–440, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Burchiel, M. A. Liker, and A. M. Lozano, “Introduction: deep brain stimulation: current assessment, new applications, and future innovations,” Neurosurgical Focus, vol. 38, no. 6, p. E1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Brunoni, M. Nitsche, and C. Loo, Transcranial Direct Current Stimulation in Neuropsychiatric Disorders: Clinical Principles and Management, Springer International Publishing, Switzerland, 2016.
  68. N. Roche, M. Geiger, and B. Bussel, “Mechanisms underlying transcranial direct current stimulation in rehabilitation,” Annals of Physical and Rehabilitation Medicine, vol. 58, no. 4, pp. 214–219, 2015. View at Publisher · View at Google Scholar · View at Scopus
  69. F. Fregni, M. A. Nitsche, C. K. Loo et al., “Regulatory considerations for the clinical and research use of transcranial direct current stimulation (tDCS): review and recommendations from an expert panel,” Clinical Research and Regulatory Affairs, vol. 32, no. 1, pp. 22–35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  70. A. M. Kuncel and W. M. Grill, “Selection of stimulus parameters for deep brain stimulation,” Clinical Neurophysiology, vol. 115, no. 11, pp. 2431–2441, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Lettieri, S. Rinaldo, G. Devigili et al., “Clinical outcome of deep brain stimulation for dystonia: constant-current or constant-voltage stimulation? A non-randomized study,” European Journal of Neurology, vol. 22, no. 6, pp. 919–926, 2015. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Chiken and A. Nambu, “Mechanism of deep brain stimulation: inhibition, excitation, or disruption?” The Neuroscientist, vol. 22, no. 3, pp. 313–322, 2016. View at Publisher · View at Google Scholar · View at Scopus
  73. T. M. Herrington, J. J. Cheng, and E. N. Eskandar, “Mechanism of deep brain stimulation,” Journal of Neurophysiology, vol. 115, no. 1, pp. 19–38, 2016. View at Publisher · View at Google Scholar · View at Scopus
  74. A. J. Fenoy, L. Goetz, S. Chabardès, and Y. Xia, “Deep brain stimulation: are astrocytes a key driver behind the scene?” CNS Neuroscience & Therapeutics, vol. 20, no. 3, pp. 191–201, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. M. A. Rueger, M. H. Keuters, M. Walberer et al., “Multi-session transcranial direct current stimulation (tDCS) elicits inflammatory and regenerative processes in the rat brain,” PloS One, vol. 7, no. 8. article e43776, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. M. H. Keuters, M. Aswendt, A. Tennstaedt et al., “Transcranial direct current stimulation promotes the mobility of engrafted NSCs in the rat brain,” NMR in Biomedicine, vol. 28, no. 2, pp. 231–239, 2015. View at Publisher · View at Google Scholar · View at Scopus
  77. R. Babona-Pilipos, A. Pritchard-Oh, M. R. Popovic, and C. M. Morshead, “Biphasic monopolar electrical stimulation induces rapid and directed galvanotaxis in adult subependymal neural precursors,” Stem Cell Research & Therapy, vol. 6, no. 1, p. 67, 2015. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Pikhovych, N. P. Stolberg, L. J. Flitsch et al., “Transcranial direct current stimulation modulates neurogenesis and microglia activation in the mouse brain,” Stem Cells International, vol. 2016, Article ID 2715196, 9 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  79. J. M. Encinas, C. Hamami, A. M. Lozano, and G. Enikolopov, “Neurogenic hippocampal targets of deep brain stimulation,” The Journal of Comparative Neurology, vol. 519, no. 1, pp. 6–20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. V. Vedam-Mai, B. Gardner, M. S. Okun et al., “Increased precursor cell proliferation after deep brain stimulation for Parkinson’s disease: a human study,” PloS One, vol. 9, no. 3, article e88770, 2014. View at Publisher · View at Google Scholar · View at Scopus
  81. D. T. Brocker and W. M. Grill, “Principles of electrical stimulation of neural tissue,” Handbook of Clinical Neurology, vol. 116, pp. 3–18, 2013. View at Publisher · View at Google Scholar · View at Scopus