Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016, Article ID 5214561, 13 pages
http://dx.doi.org/10.1155/2016/5214561
Research Article

Shrimp Protein Hydrolysate Modulates the Timing of Proinflammatory Macrophages in Bupivacaine-Injured Skeletal Muscles in Rats

1School of Nutrition, Laval University, Quebec City, QC, Canada G1V 0A6
2Institute of Nutraceuticals and Functional Foods, Laval University, Quebec City, QC, Canada G1V 0A6
3Merinov, Quebec Fisheries and Aquaculture Innovation Centre, 96 montée de Sandy Beach, Office 1.07, Gaspé, QC, Canada G4X 2V6
4ISMER, Université du Québec à Rimouski, 300 allée des Ursulines, P.O. Box 3300, Rimouski, QC, Canada G5L 3A1
5Quebec Agrifood Development Center, La Pocatière, QC, Canada

Received 7 July 2016; Revised 14 September 2016; Accepted 28 September 2016

Academic Editor: Cristina Martínez-Villaluenga

Copyright © 2016 Junio Dort 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. P. K. Shireman, V. Contreras-Shannon, O. Ochoa, B. P. Karia, J. E. Michalek, and L. M. McManus, “MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration,” Journal of Leukocyte Biology, vol. 81, no. 3, pp. 775–785, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. B. M. Lapointe, J. Frenette, and C. H. Côté, “Lengthening contraction-induced inflammation is linked to secondary damage but devoid of neutrophil invasion,” Journal of Applied Physiology, vol. 92, no. 5, pp. 1995–2004, 2002. View at Google Scholar · View at Scopus
  3. J. Dort, N. Leblanc, J. Maltais-Giguère, B. Liaset, C. H. Côté, and H. Jacques, “Beneficial effects of cod protein on inflammatory cell accumulation in rat skeletal muscle after injury are driven by its high levels of arginine, glycine, taurine and lysine,” PLoS ONE, vol. 8, no. 10, article e77274, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. J. G. Tidball, “Mechanisms of muscle injury, repair, and regeneration,” American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 1, no. 4, pp. 2029–2062, 2029. View at Google Scholar
  5. J. G. Tidball and S. A. Villalta, “Regulatory interactions between muscle and the immune system during muscle regeneration,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 298, no. 5, pp. R1173–R1187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Wehling, M. J. Spencer, and J. G. Tidball, “A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice,” Journal of Cell Biology, vol. 155, no. 1, pp. 123–131, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Kyriakides, W. Austen Jr., Y. Wang et al., “Skeletal muscle reperfusion injury is mediated by neutrophils and the complement membrane attack complex,” American Journal of Physiology—Cell Physiology, vol. 277, no. 6, pp. C1263–C1268, 1999. View at Google Scholar · View at Scopus
  8. P. A. Harnedy and R. J. FitzGerald, “Bioactive peptides from marine processing waste and shellfish: a review,” Journal of Functional Foods, vol. 4, no. 1, pp. 6–24, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Dort, A. Sirois, N. Leblanc, C. H. Côté, and H. Jacques, “Beneficial effects of cod protein on skeletal muscle repair following injury,” Applied Physiology, Nutrition and Metabolism, vol. 37, no. 3, pp. 489–498, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Pilon, J. Ruzzin, L.-E. Rioux et al., “Differential effects of various fish proteins in altering body weight, adiposity, inflammatory status, and insulin sensitivity in high-fat-fed rats,” Metabolism: Clinical and Experimental, vol. 60, no. 8, pp. 1122–1130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. I. Rudkowska, B. Marcotte, G. Pilon, C. Lavigne, A. Marette, and M.-C. Vohl, “Fish nutrients decrease expression levels of tumor necrosis factor-α in cultured human macrophages,” Physiological Genomics, vol. 40, no. 3, pp. 189–194, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Dort, N. Leblanc, C. H. Côté, and H. Jacques, “Dietary cod protein improves the IGF1-Akt/PKB signaling pathway in rat skeletal muscle during recovery from injury,” The FASEB Journal, vol. 27, supplement, no. 1, p. 631.13, 2013. View at Google Scholar
  13. E. Mente, P. Coutteau, D. Houlihan, I. Davidson, and P. Sorgeloos, “Protein turnover, amino acid profile and amino acid flux in juvenile shrimp Litopenaeus vannamei: effects of dietary protein source,” Journal of Experimental Biology, vol. 205, no. 20, pp. 3107–3122, 2002. View at Google Scholar · View at Scopus
  14. F. J. Alarcon-Aguilar, J. Almanza-Perez, G. Blancas et al., “Glycine regulates the production of pro-inflammatory cytokines in lean and monosodium glutamate-obese mice,” European Journal of Pharmacology, vol. 599, no. 1, pp. 152–158, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Hnia, J. Gayraud, G. Hugon et al., “l-arginine decreases inflammation and modulates the nuclear factor-κB/matrix metalloproteinase cascade in mdx muscle fibers,” The American Journal of Pathology, vol. 172, no. 6, pp. 1509–1519, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. L. A. Silva, P. C. L. Silveira, M. M. Ronsani et al., “Taurine supplementation decreases oxidative stress in skeletal muscle after eccentric exercise,” Cell Biochemistry and Function, vol. 29, no. 1, pp. 43–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. S. W. Schaffer, J. Azuma, and M. Mozaffari, “Role of antioxidant activity of taurine in diabetes,” Canadian Journal of Physiology and Pharmacology, vol. 87, no. 2, pp. 91–99, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Schaefer, K. Tahara, S. Schuchtrup et al., “Perioperative glycine treatment attenuates ischemia/reperfusion injury and ameliorates smooth muscle dysfunction in intestinal transplantation,” Transplantation, vol. 85, no. 9, pp. 1300–1310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. P. G. Reeves, F. H. Nielsen, and G. C. Fahey Jr., “AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet,” Journal of Nutrition, vol. 123, no. 11, pp. 1939–1951, 1993. View at Google Scholar · View at Scopus
  20. L. Beaulieu, J. Thibodeau, C. Bonnet, P. Bryl, and M.-É. Carbonneau, “Detection of antibacterial activity in an enzymatic hydrolysate fraction obtained from processing of Atlantic rock crab (Cancer irroratus) by-products,” PharmaNutrition, vol. 1, no. 4, pp. 149–157, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. D. I. Sánchez-Machado, B. Chavira-Willys, and J. López-Cervantes, “High-performance liquid chromatography with fluorescence detection for quantitation of tryptophan and tyrosine in a shrimp waste protein concentrate,” Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences, vol. 863, no. 1, pp. 88–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. E. C. B. Hall-Craggs, “Early ultrastructural changes in skeletal muscle exposed to the local anaesthetic bupivacaine (Marcaine),” British Journal of Experimental Pathology, vol. 61, no. 2, pp. 139–149, 1980. View at Google Scholar · View at Scopus
  23. F. X. Pizza, J. M. Peterson, J. H. Baas, and T. J. Koh, “Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice,” Journal of Physiology, vol. 562, no. 3, pp. 899–913, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Smith, M. J. Kruger, R. M. Smith, and K. H. Myburgh, “The inflammatory response to skeletal muscle injury: illuminating complexities,” Sports Medicine, vol. 38, no. 11, pp. 947–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Gregorevic, D. R. Plant, N. Stupka, and G. S. Lynch, “Changes in contractile activation characteristics of rat fast and slow skeletal muscle fibres during regeneration,” Journal of Physiology, vol. 558, no. 2, pp. 549–560, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. S. A. Villalta, C. Rinaldi, B. Deng, G. Liu, B. Fedor, and J. G. Tidball, “Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype,” Human Molecular Genetics, vol. 20, no. 4, pp. 790–805, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Arnold, A. Henry, F. Poron et al., “Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 1057–1069, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Chazaud, M. Brigitte, H. Yacoub-Youssef et al., “Dual and beneficial roles of macrophages during skeletal muscle regeneration,” Exercise and Sport Sciences Reviews, vol. 37, no. 1, pp. 18–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Wang, D. W. Melton, L. Porter, Z. U. Sarwar, L. M. McManus, and P. K. Shireman, “Altered macrophage phenotype transition impairs skeletal muscle regeneration,” American Journal of Pathology, vol. 184, no. 4, pp. 1167–1184, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Cantini, M. L. Massimino, A. Bruson, C. Catani, L. Dalla Libera, and U. Carraro, “Macrophages regulate proliferation and differentiation of satellite cells,” Biochemical and Biophysical Research Communications, vol. 202, no. 3, pp. 1688–1696, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. R. D. Stout, C. Jiang, B. Matta, I. Tietzel, S. K. Watkins, and J. Suttles, “Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences,” Journal of Immunology, vol. 175, no. 1, pp. 342–349, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Buechler, M. Ritter, E. Orsó, T. Langmann, J. Klucken, and G. Schmitz, “Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli,” Journal of Leukocyte Biology, vol. 67, no. 1, pp. 97–103, 2000. View at Google Scholar · View at Scopus
  33. A. Gratchev, J. Kzhyshkowska, K. Köthe et al., “Mφ1 and Mφ2 can be re-polarized by Th2 or Th1 cytokines, respectively, and respond to exogenous danger signals,” Immunobiology, vol. 2011, no. 6–8, pp. 473–486, 2006. View at Google Scholar
  34. A. R. Burns, Z. Zheng, S. H. Soubra, J. Chen, and R. E. Rumbaut, “Transendothelial flow inhibits neutrophil transmigration through a nitric oxide-dependent mechanism: potential role for cleft shear stress,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 293, no. 5, pp. H2904–H2910, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Kubes, M. Suzuki, and D. N. Granger, “Nitric oxide: an endogenous modulator of leukocyte adhesion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 11, pp. 4651–4655, 1991. View at Publisher · View at Google Scholar · View at Scopus
  36. D. J. Lefer, S. P. Jones, W. G. Girod et al., “Leukocyte-endothelial cell interactions in nitric oxide synthase- deficient mice,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 276, no. 6, pp. H1943–H1950, 1999. View at Google Scholar · View at Scopus
  37. B. Stoffels, A. Türler, J. Schmidt et al., “Anti-inflammatory role of glycine in reducing rodent postoperative inflammatory ileus,” Neurogastroenterology and Motility, vol. 23, no. 1, pp. 76–87, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. I. H. C. Vos, T. J. Rabelink, B. Dorland et al., “L-arginine supplementation improves function and reduces inflammation in renal allografts,” Journal of the American Society of Nephrology, vol. 12, no. 2, pp. 361–367, 2001. View at Google Scholar · View at Scopus
  39. Y.-H. Nong, R. G. Titus, J. M. C. Ribeiro, and H. G. Remold, “Peptides encoded by the calcitonin gene inhibit macrophage function,” Journal of Immunology, vol. 143, no. 1, pp. 45–49, 1989. View at Google Scholar · View at Scopus
  40. M. Li, C. Li, and W. S. Parkhouse, “Age-related differences in the des IGF-I-mediated activation of Akt-1 and p70 S6K in mouse skeletal muscle,” Mechanisms of Ageing and Development, vol. 124, no. 7, pp. 771–778, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Jacques, N. Leblanc, R. Papineau, D. Richard, and C. H. Côté, “Peanut protein reduces body protein mass and alters skeletal muscle contractile properties and lipid metabolism in rats,” British Journal of Nutrition, vol. 103, no. 9, pp. 1331–1339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. G. S. Gilani, W. M. N. Ratnayake, R. W. Peace, and R. Mueller, “Effects of supplemental cystine or methionine on growth and lifespan of stroke-prone spontaneously hypertensive rats,” British Journal of Nutrition, vol. 95, no. 3, pp. 443–447, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Paddon-Jones, M. Sheffield-Moore, R. J. Urban et al., “Essential amino acid and carbohydrate supplementation ameliorates muscle protein loss in humans during 28 days bedrest,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 9, pp. 4351–4358, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. C. M. Ross-Inta, Y.-F. Zhang, A. Almendares, and C. Giulivi, “Threonine-deficient diets induced changes in hepatic bioenergetics,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 296, no. 5, pp. G1130–G1139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Boirie, M. Dangin, P. Gachon, M.-P. Vasson, J.-L. Maubois, and B. Beaufrère, “Slow and fast dietary proteins differently modulate postprandial protein accretion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 26, pp. 14930–14935, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. J. G. Tidball, “Inflammatory processes in muscle injury and repair,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 288, no. 2, pp. R345–R353, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. A. R. Spitze, D. L. Wong, Q. R. Rogers, and A. J. Fascetti, “Taurine concentrations in animal feed ingredients; cooking influences taurine content,” Journal of Animal Physiology and Animal Nutrition, vol. 87, no. 7-8, pp. 251–262, 2003. View at Publisher · View at Google Scholar · View at Scopus