A perspective on immunomodulation and tissue repair

Annals of Biomedical Engineering

Volumn 42, Issue 2, 2014, Pages 338-351

  Mokarram, Nassir ^a   Bellamkonda, Ravi V ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Biomaterials; Immunomodulation; Macrophage; Monocyte; Wound healing

Indexed keywords

BIOMATERIALS; BODY FLUIDS; TISSUE REGENERATION;

IMMUNE RESPONSE; IMMUNO MODULATIONS; MONOCYTE; REGENERATIVE MEDICINE; TISSUE REPAIR; TISSUE TYPES; WOUND HEALING;

MACROPHAGES;

BIOMATERIAL;

CELL ACTIVITY; CONFERENCE PAPER; HEART; HUMAN; IMMUNOMODULATION; MACROPHAGE; MONOCYTE; MUSCLE INJURY; MUSCLE TISSUE; NERVOUS TISSUE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; SKIN; TISSUE ENGINEERING; TISSUE INJURY; TISSUE REGENERATION; TISSUE REPAIR; WOUND HEALING;

ANIMALS; BIOCOMPATIBLE MATERIALS; HUMANS; IMMUNOMODULATION; MACROPHAGES; MONOCYTES; WOUND HEALING;

EID: 84899410605     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-013-0941-0     Document Type: Conference Paper

References (111)

1. Adamson, R. Role of macrophages in normal wound healing: an overview. J. Wound Care 18:349-351, 2009.
2. Arnold, L., A. Henry, F. Poron, Y. Baba-Amer, N. Van Rooijen, A. Plonquet, R. K. Gherardi, and B. Chazaud. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204:1057-1069, 2007.
3. Auffray, C., M. H. Sieweke, and F. Geissmann. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27:669-692, 2009.
4. Awojoodu, A. O., M. E. Ogle, L. S. Sefcik, D. T. Bowers, K. Martin, K. L. Brayman, K. R. Lynch, S. M. Peirce-Cottler, and E. Botchwey. Sphingosine 1-phosphate receptor 3 regulates recruitment of anti-inflammatory monocytes to microvessels during implant arteriogenesis. Proc. Natl Acad. Sci. U. S. A. 110:13785-13790, 2013.
5. Badylak, S. F., J. E. Valentin, A. K. Ravindra, G. P. McCabe, and A. M. Stewart-Akers. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng. Part A 14:1835-1842, 2008.
6. Barminko, J., J. H. Kim, S. Otsuka, A. Gray, R. Schloss, M. Grumet, and M. L. Yarmush. Encapsulated mesenchymal stromal cells for in vivo transplantation. Biotechnol. Bioeng. 108:2747-2758, 2011.
7. Barrientos, S., O. Stojadinovic, M. S. Golinko, H. Brem, and M. Tomic-Canic. Growth factors and cytokines in wound healing. Wound Repair Regen. 16:585-601, 2008.
8. Barth, K. A., J. D. Waterfield, and D. M. Brunette. The effect of surface roughness on RAW 264.7 macrophage phenotype. J. Biomed. Mater. Res. A 101:2679-88, 2013.
9. Bartneck, M., K.-H. Heffels, Y. Pan, M. Bovi, G. Zwadlo-Klarwasser, and J. Groll. Inducing healing-like human primary macrophage phenotypes by 3D hydrogel coated nanofibres. Biomaterials 33:4136-4146, 2012.
10. Bellingan, G. J., P. Xu, H. Cooksley, H. Cauldwell, A. Shock, S. Bottoms, C. Haslett, S. E. Mutsaers, and G. J. Laurent. Adhesion molecule-dependent mechanisms regulate the rate of macrophage clearance during the resolution of peritoneal inflammation. J. Exp. Med. 196:1515-1521, 2002.
11. Besser, M., and R. Wank. Cutting edge: clonally restricted production of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 mRNA by human immune cells and Th1/Th2-polarized expression of their receptors. J. Immunol. 162:6303-6306, 1999.
12. Blakney, A. K., M. D. Swartzlander, and S. J. Bryant. The effects of substrate stiffness on the in vitro activation of macrophages and in vivo host response to poly (ethylene glycol)-based hydrogels. J. Biomed. Mater. Res. A 100:1375-1386, 2012.
13. Bomstein, Y., J. B. Marder, K. Vitner, I. Smirnov, G. Lisaey, O. Butovsky, V. Fulga, and E. Yoles. Features of skin-coincubated macrophages that promote recovery from spinal cord injury. J. Neuroimmunol. 142:10-16, 2003.
14. Bota, P. C. S., A. M. B. Collie, P. Puolakkainen, R. B. Vernon, E. H. Sage, B. D. Ratner, and P. S. Stayton. Biomaterial topography alters healing in vivo and monocyte/macrophage activation in vitro. J. Biomed. Mater. Res. A 95:649-657, 2010.
15. Brown, B. N., and S. F. Badylak. Expanded applications, shifting paradigms and an improved understanding of host-biomaterial interactions. Acta Biomater. 9:4948-4955, 2013.
16. Brown, B. N., R. Londono, S. Tottey, L. Zhang, K. A. Kukla, M. T. Wolf, K. A. Daly, J. E. Reing, and S. F. Badylak. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater. 8:978-987, 2012.
17. Brown, B. N., B. D. Ratner, S. B. Goodman, S. Amar, and S. F. Badylak. Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials 33:3792-3802, 2012.
18. Bryers, J. D., C. M. Giachelli, and B. D. Ratner. Engineering biomaterials to integrate and heal: the biocompatibility paradigm shifts. Biotechnol. Bioeng. 109:1898-1911, 2012.
19. Charriere, G. M., B. Cousin, E. Arnaud, C. Saillan-Barreau, M. Andre, A. Massoudi, C. Dani, L. Penicaud, and L. Casteilla. Macrophage characteristics of stem cells revealed by transcriptome profiling. Exp. Cell Res. 312:3205-3214, 2006.
20. Chen, S., J. A. Jones, Y. Xu, H.-Y. Low, J. M. Anderson, and K. W. Leong. Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31:3479-3491, 2010.
21. Chien, K. R., I. J. Domian, and K. K. Parker. Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 322:1494-1497, 2008.
22. Das, A., C. E. Segar, B. B. Hughley, D. T. Bowers, and E. A. Botchwey. The promotion of mandibular defect healing by the targeting of S1P receptors and the recruitment of alternatively activated macrophages. Biomaterials 34:9853-9862, 2013.
23. De Simone, R., E. Ambrosini, D. Carnevale, M. A. Ajmone-Cat, and L. Minghetti. NGF promotes microglial migration through the activation of its high affinity receptor: modulation by TGF-beta. J. Neuroimmunol. 190:53-60, 2007.
24. Deboy, C. A, J. Xin, S. C. Byram, C. J. Serpe, V. M. Sanders, and K. J. Jones. Immune-mediated neuroprotection of axotomized mouse facial motoneurons is dependent on the IL-4/STAT6 signaling pathway in CD4 (+) T cells. Exp. Neurol. 201:212-224, 2006.
25. Deonarine, K., M. C. Panelli, M. E. Stashower, P. Jin, K. Smith, H. B. Slade, C. Norwood, E. Wang, F. M. Marincola, and D. F. Stroncek. Gene expression profiling of cutaneous wound healing. J. Transl. Med. 5:11, 2007.
26. Dewald, O., P. Zymek, K. Winkelmann, A. Koerting, G. Ren, T. Abou-Khamis, L. H. Michael, B. J. Rollins, M. L. Entman, and N. G. Frangogiannis. CCL2/Monocyte Chemoattractant Protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ. Res. 96:881-889, 2005.
27. Fadok, V. A., P. P. McDonald, D. L. Bratton, and P. M. Henson. Regulation of macrophage cytokine production by phagocytosis of apoptotic and post-apoptotic cells. Biochem. Soc. Trans. 26:653-656, 1998.
28. Fraccarollo, D., P. Galuppo, and J. Bauersachs. Novel therapeutic approaches to post-infarction remodelling. Cardiovasc. Res. 94:293-303, 2012.
29. Franz, S., S. Rammelt, D. Scharnweber, and J. C. Simon. Immune responses to implants-a review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32:6692-6709, 2011.
30. Fukano, Y., M. L. Usui, R. A. Underwood, S. Isenhath, A. J. Marshall, K. D. Hauch, B. D. Ratner, J. E. Olerud, and P. Fleckman. Epidermal and dermal integration into sphere-templated porous poly (2-hydroxyethyl methacrylate) implants in mice. J. Biomed. Mater. Res. A 94:1172-1186, 2010.
31. Gaudet, A. D., P. G. Popovich, and M. S. Ramer. Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J. Neuroinflammation 8:110, 2011.
32. Geissmann, F., M. G. Manz, S. Jung, M. H. Sieweke, M. Merad, and K. Ley. Development of monocytes, macrophages, and dendritic cells. Science 327:656-661, 2010.
33. Gensel, J. C., S. Nakamura, Z. Guan, N. Van Rooijen, D. P. Ankeny, and P. G. Popovich. Macrophages promote axon regeneration with concurrent neurotoxicity. J. Neurosci. 29:3956-3968, 2009.
34. Gerstein, A. D., T. J. Phillips, G. S. Rogers, and B. A. Gilchrest. Wound healing and aging. Dermatol. Clin. 11:749-757, 1993.
35. Godwin, J. W., A. R. Pinto, and N. A. Rosenthal. Macrophages are required for adult salamander limb regeneration. Proc. Natl Acad. Sci. 110:9415-9420, 2013.
36. Goh, Y. P. S., N. C. Henderson, J. E. Heredia, A. Red Eagle, J. I. Odegaard, N. Lehwald, K. D. Nguyen, D. Sheppard, L. Mukundan, R. M. Locksley, and A. Chawla. Eosinophils secrete IL-4 to facilitate liver regeneration. Proc. Natl Acad. Sci. U. S. A. 110:9914-9919, 2013.
37. Gordon, S. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23-35, 2003.
38. Gordon, S., and P. R. Taylor. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964, 2005.
39. Harel-Adar, T., T. Ben Mordechai, Y. Amsalem, M. S. Feinberg, J. Leor, and S. Cohen. Modulation of cardiac macrophages by phosphatidylserine-presenting liposomes improves infarct repair. Proc. Natl Acad. Sci. U. S. A. 108:1827-1832, 2011.
40. Hughes, J. E., S. Srinivasan, K. R. Lynch, R. L. Proia, P. Ferdek, and C. C. Hedrick. Sphingosine-1-phosphate induces an antiinflammatory phenotype in macrophages. Circ. Res. 102:950-958, 2008.
41. Janssens, S., K. Burns, J. Tschopp, and R. Beyaert. Regulation of interleukin-1- and lipopolysaccharide-induced NF-kappaB activation by alternative splicing of MyD88. Curr. Biol. 12:467-471, 2002.
42. Jenkins, S. J., D. Ruckerl, P. C. Cook, L. H. Jones, F. D. Finkelman, N. Van Rooijen, A. S. MacDonald, and J. E. Allen. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332:1284-1288, 2011.
43. Kaikita, K., T. Hayasaki, T. Okuma, W. A. Kuziel, H. Ogawa, and M. Takeya. Targeted deletion of CC chemokine receptor 2 attenuates left ventricular remodeling after experimental myocardial infarction. Am. J. Pathol. 165:439-447, 2004.
44. Kigerl, K. A., J. C. Gensel, D. P. Ankeny, J. K. Alexander, D. J. Donnelly, and P. G. Popovich. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 29:13435-13444, 2009.
45. Kim, J., and P. Hematti. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp. Hematol. 37:1445-1453, 2009.
46. Landesman-Milo, D., and D. Peer. Altering the immune response with lipid-based nanoparticles. J. Control. Release 161:600-608, 2012.
47. Lazarov-Spiegler, O., A. S. Solomon, A. B. Zeev-Brann, D. L. Hirschberg, V. Lavie, and M. Schwartz. Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J. 10:1296-1302, 1996.
48. Lee, R. H., A. A. Pulin, M. J. Seo, D. J. Kota, J. Ylostalo, B. L. Larson, L. Semprun-Prieto, P. Delafontaine, and D. J. Prockop. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5:54-63, 2009.
49. Leuschner, F., P. Dutta, R. Gorbatov, T. I. Novobrantseva, J. S. Donahoe, G. Courties, K. M. Lee, J. I. Kim, J. F. Markmann, B. Marinelli, P. Panizzi, W. W. Lee, Y. Iwamoto, S. Milstein, H. Epstein-Barash, W. Cantley, J. Wong, V. Cortez-Retamozo, A. Newton, K. Love, P. Libby, M. J. Pittet, F. K. Swirski, V. Koteliansky, R. Langer, R. Weissleder, D. G. Anderson, and M. Nahrendorf. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 29:1005-1010, 2011.
50. Leuschner, F., P. J. Rauch, T. Ueno, R. Gorbatov, B. Marinelli, W. W. Lee, P. Dutta, Y. Wei, C. Robbins, Y. Iwamoto, B. Sena, A. Chudnovskiy, P. Panizzi, E. Keliher, J. M. Higgins, P. Libby, M. A. Moskowitz, M. J. Pittet, F. K. Swirski, R. Weissleder, and M. Nahrendorf. Rapid monocyte kinetics in acute myocardial infarction are sustained by extramedullary monocytopoiesis. J. Exp. Med. 209:123-137, 2012.
51. Li, Y.-P. TNF-alpha is a mitogen in skeletal muscle. Am. J. Physiol. Cell Physiol. 285:C370-C376, 2003.
52. Liu, Y., Y. Hu, Y. Guo, H. Ma, J. Li, and C. Jiang. Targeted imaging of activated caspase-3 in the central nervous system by a dual functional nano-device. J. Control. Release 163:203-210, 2012.
53. Lolmede, K., L. Campana, M. Vezzoli, L. Bosurgi, R. Tonlorenzi, E. Clementi, M. E. Bianchi, G. Cossu, A. A. Manfredi, S. Brunelli, and P. Rovere-Querini. Inflammatory and alternatively activated human macrophages attract vessel-associated stem cells, relying on separate HMGB1- and MMP-9-dependent pathways. J. Leukoc. Biol. 85:779-787, 2009.
54. Lucas, T., A. Waisman, R. Ranjan, J. Roes, T. Krieg, W. Muller, A. Roers, and S. A. Eming. Differential roles of macrophages in diverse phases of skin repair. J. Immunol. 184:3964-3977, 2010.
55. Madden, L. R., D. J. Mortisen, E. M. Sussman, S. K. Dupras, J. A. Fugate, J. L. Cuy, K. D. Hauch, M. A. Laflamme, C. E. Murry, and B. D. Ratner. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc. Natl Acad. Sci. U. S. A. 107:15211-15216, 2010.
56. Mahbub, S., C. R. Deburghgraeve, and E. J. Kovacs. Advanced age impairs macrophage polarization. J. Interferon Cytokine Res. 32:18-26, 2012.
57. Majmudar, M. D., E. J. Keliher, T. Heidt, F. Leuschner, J. Truelove, B. F. Sena, R. Gorbatov, Y. Iwamoto, P. Dutta, G. Wojtkiewicz, G. Courties, M. Sebas, A. Borodovsky, K. Fitzgerald, M. W. Nolte, G. Dickneite, J. W. Chen, D. G. Anderson, F. K. Swirski, R. Weissleder, and M. Nahrendorf. Monocyte-directed RNAi targeting CCR2 improves infarct healing in atherosclerosis-prone mice. Circulation 127:2038-2046, 2013.
58. Mantovani, A., S. K. Biswas, M. R. Galdiero, A. Sica, and M. Locati. Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229:176-185, 2013.
59. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677-686, 2004.
60. Mirza, R., L. A. Di Pietro, and T. J. Koh. Selective and specific macrophage ablation is detrimental to wound healing in mice. Am. J. Pathol. 175:2454-2462, 2009.
61. Mokarram, N., and R. V Bellamkonda. Overcoming endogenous constraints on neuronal regeneration. IEEE Trans. Biomed. Eng. 58:1900-1906, 2011.
62. Mokarram, N., A. Merchant, V. Mukhatyar, G. Patel, and R. V. Bellamkonda. Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials 33:8793-8801, 2012.
63. Mosser, D. M., and J. P. Edwards. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8:958-969, 2008.
64. Mukhatyar, V., L. Karumbaiah, J. Yeh, and R. Bellamkonda. Tissue engineering strategies designed to realize the endogenous regenerative potential of peripheral nerves. Adv. Mater. 21:4670-4679, 2009.
65. Mullarky, I. K., F. M. Szaba, K. N. Berggren, L. W. Kummer, L. B. Wilhelm, M. A. Parent, L. L. Johnson, and S. T. Smiley. Tumor necrosis factor alpha and gamma interferon, but not hemorrhage or pathogen burden, dictate levels of protective fibrin deposition during infection. Infect. Immun. 74:1181-1188, 2006.
66. Murray, P. J., and T. A. Wynn. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11:723-737, 2011.
67. Nahrendorf, M., M. J. Pittet, and F. K. Swirski. Monocytes: protagonists of infarct inflammation and repair after myocardial infarction. Circulation 121:2437-2445, 2010.
68. Nahrendorf, M., F. K. Swirski, E. Aikawa, L. Stangenberg, T. Wurdinger, J.-L. Figueiredo, P. Libby, R. Weissleder, and M. J. Pittet. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 204:3037-3047, 2007.
69. Nakajima, H., K. Uchida, A. R. Guerrero, S. Watanabe, D. Sugita, N. Takeura, A. Yoshida, G. Long, K. T. Wright, W. E. B. Johnson, and H. Baba. Transplantation of mesenchymal stem cells promotes an alternative pathway of macrophage activation and functional recovery after spinal cord injury. J. Neurotrauma 29:1614-1625, 2012.
70. Olefsky, J. M., and C. K. Glass. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72:219-246, 2010.
71. Onofre, G., M. Kolackova, K. Jankovicova, and J. Krejsek. Scavenger receptor CD163 and its biological functions. Acta Medica (Hradec Kralove) 52:57-61, 2009.
72. Park, J. E., and A. Barbul. Understanding the role of immune regulation in wound healing. Am. J. Surg. 187:11S-16S, 2004.
73. Paul, N. E., C. Skazik, M. Harwardt, M. Bartneck, B. Denecke, D. Klee, J. Salber, and G. Zwadlo-Klarwasser. Topographical control of human macrophages by a regularly microstructured polyvinylidene fluoride surface. Biomaterials 29:4056-4064, 2008.
74. St Pierre, B. A., and J. G. Tidball. Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J. Appl. Physiol. 77:290-297, 1994.
75. Porcheray, F., S. Viaud, A.-C. Rimaniol, C. Leone, B. Samah, N. Dereuddre-Bosquet, D. Dormont, and G. Gras. Macrophage activation switching: an asset for the resolution of inflammation. Clin. Exp. Immunol. 142:481-489, 2005.
76. Rao, A. J., E. Gibon, T. Ma, Z. Yao, R. L. Smith, and S. B. Goodman. Revision joint replacement, wear particles, and macrophage polarization. Acta Biomater. 8:2815-2823, 2012.
77. Rao, A. J., C. Nich, L. S. Dhulipala, E. Gibon, R. Valladares, S. Zwingenberger, R. L. Smith, and S. B. Goodman. Local effect of IL-4 delivery on polyethylene particle induced osteolysis in the murine calvarium. J. Biomed. Mater. Res. A 101:1926-1934, 2013.
78. Rapalino, O., O. Lazarov-Spiegler, E. Agranov, G. J. Velan, E. Yoles, M. Fraidakis, A. Solomon, R. Gepstein, A. Katz, M. Belkin, M. Hadani, and M. Schwartz. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat. Med. 4:814-821, 1998.
79. Redd, M. J., L. Cooper, W. Wood, B. Stramer, and P. Martin. Wound healing and inflammation: embryos reveal the way to perfect repair. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359:777-784, 2004.
80. Rodero, M. P., and K. Khosrotehrani. Skin wound healing modulation by macrophages. Int. J. Clin. Exp. Pathol. 3:643-653, 2010.
81. Rolls, A., R. Shechter, and M. Schwartz. The bright side of the glial scar in CNS repair. Nat. Rev. Neurosci. 10:235-241, 2009.
82. Schwartz, M. "Tissue-repairing" blood-derived macrophages are essential for healing of the injured spinal cord: from skin-activated macrophages to infiltrating blood-derived cells? Brain. Behav. Immun. 24:1054-1057, 2010.
83. Serrano, A. L., B. Baeza-Raja, E. Perdiguero, M. Jardi, and P. Munoz-Canoves. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 7:33-44, 2008.
84. Seta, N., and M. Kuwana. Derivation of multipotent progenitors from human circulating CD14+ monocytes. Exp. Hematol. 38:557-563, 2010.
85. Shechter, R., A. London, and M. Schwartz. Orchestrated leukocyte recruitment to immune-privileged sites: absolute barriers versus educational gates. Nat. Rev. Immunol. 13:206-218, 2013.
86. Shechter, R., A. London, C. Varol, C. Raposo, M. Cusimano, G. Yovel, A. Rolls, M. Mack, S. Pluchino, G. Martino, S. Jung, and M. Schwartz. Infiltrating blood-derived macrophages are vital cells playing an antiinflammatory role in recovery from spinal cord injury in mice. PLoS Med. 6:e1000113, 2009.
87. Shi, C., and E. G. Pamer. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11:762-774, 2011.
88. Stout, R. D., 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. J. Immunol. 175:342-349, 2005.
89. Stout, R. D., and J. Suttles. Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J. Leukoc. Biol. 76:509-513, 2004.
90. Strle, K., R. H. McCusker, L. Tran, A. King, R. W. Johnson, G. G. Freund, R. Dantzer, and K. W. Kelley. Novel activity of an anti-inflammatory cytokine: IL-10 prevents TNFalpha-induced resistance to IGF-I in myoblasts. J. Neuroimmunol. 188:48-55, 2007.
91. Summan, M., G. L. Warren, R. R. Mercer, R. Chapman, T. Hulderman, N. Van Rooijen, and P. P. Simeonova. Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R1488-R1495, 2006.
92. Szalay, K., Z. Razga, and E. Duda. TNF inhibits myogenesis and downregulates the expression of myogenic regulatory factors myoD and myogenin. Eur. J. Cell Biol. 74:391-398, 1997.
93. Tidball, J. G., and S. A. Villalta. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298:R1173-R1187, 2010.
94. Tidball, J. G., and M. Wehling-Henricks. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J. Physiol. 578:327-336, 2007.
95. Torrente, Y., E. El Fahime, N. J. Caron, R. Del Bo, M. Belicchi, F. Pisati, J. P. Tremblay, and N. Bresolin. Tumor necrosis factor-alpha (TNF-alpha) stimulates chemotactic response in mouse myogenic cells. Cell Transplant. 12:91-100, 2003.
96. Tsou, C.-L., W. Peters, Y. Si, S. Slaymaker, A. M. Aslanian, S. P. Weisberg, M. Mack, and I. F. Charo. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117:902-909, 2007.
97. Tsujinaka, T., J. Fujita, C. Ebisui, M. Yano, E. Kominami, K. Suzuki, K. Tanaka, A. Katsume, Y. Ohsugi, H. Shiozaki, and M. Monden. Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. J. Clin. Invest. 97:244-249, 1996.
98. Uceyler, N., A. Tscharke, and C. Sommer. Early cytokine gene expression in mouse CNS after peripheral nerve lesion. Neurosci. Lett. 436:259-264, 2008.
99. Underwood, R. A., M. L. Usui, G. Zhao, K. D. Hauch, M. M. Takeno, B. D. Ratner, A. J. Marshall, X. Shi, J. E. Olerud, and P. Fleckman. Quantifying the effect of pore size and surface treatment on epidermal incorporation into percutaneously implanted sphere-templated porous biomaterials in mice. J. Biomed. Mater. Res. A 98:499-508, 2011.
100. Van Den Bossche, J., P. Bogaert, J. Van Hengel, C. J. Guerin, G. Berx, K. Movahedi, R. Van Den Bergh, A. Pereira-Fernandes, J. M. C. Geuns, H. Pircher, P. Dorny, J. Grooten, P. De Baetselier, and J. A. Van Ginderachter. Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamineinduced E-cadherin/catenin complexes. Blood 114:4664-4674, 2009.
101. Vidal, P. M., E. Lemmens, D. Dooley, and S. Hendrix. The role of "anti-inflammatory" cytokines in axon regeneration. Cytokine Growth Factor Rev. 24:1-12, 2013.
102. Villalta, S. A., B. Deng, C. Rinaldi, M. Wehling-Henricks, and J. G. Tidball. IFN-γ promotes muscle damage in the mdx mouse model of Duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation. J. Immunol. 187:5419-5428, 2011.
103. Villalta, S. A., H. X. Nguyen, B. Deng, T. Gotoh, and J. G. Tidball. Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet. 18:482-496, 2009.
104. Wang, Y., R. Zhou, N. Wu, Y. Mou, R. Li, and Z. Deng. Interleukin-4 and osteoprotegerin suppress polyethylene wear debris-induced osteolysis in a murine air pouch model. Nan Fang Yi Ke Da Xue Xue Bao 31:1709-1713, 2011.
105. Wehling, M., M. J. Spencer, and J. G. Tidball. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 155:123-131, 2001.
106. Schwartz, M., and E. Yoles. Immune-based therapy for spinal cord repair: autologous macrophages and beyond. J. Neurotrauma 23:360-370.
107. Ydens, E., A. Cauwels, B. Asselbergh, S. Goethals, L. Peeraer, G. Lornet, L. Almeida-Souza, J. A Van Ginderachter, V. Timmerman, and S. Janssens. Acute injury in the peripheral nervous system triggers an alternative macrophage response. J. Neuroinflammation 9:176, 2012.
108. Zhao, Y., D. Glesne, and E. Huberman. A human peripheral blood monocyte-derived subset acts as pluripotent stem cells. Proc. Natl Acad. Sci. U. S. A. 100:2426-2431, 2003.
109. Ziegler-Heitbrock, L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 81:584-592, 2007.
110. Zimmermann, H. W., S. Seidler, J. Nattermann, N. Gassler, C. Hellerbrand, A. Zernecke, J. J. W. Tischendorf, T. Luedde, R. Weiskirchen, C. Trautwein, and F. Tacke. Functional contribution of elevated circulating and hepatic non-classical CD14CD16 monocytes to inflammation and human liver fibrosis. PLoS One 5:e11049, 2010.
111. Ziv, Y., H. Avidan, S. Pluchino, G. Martino, and M. Schwartz. Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc. Natl Acad. Sci. U. S. A. 103:13174-13179, 2006.