Chasing the recipe for a pro-regenerative immune system

Seminars in Cell and Developmental Biology

Volumn 61, Issue , 2017, Pages 71-79

  Godwin, James W ^a,b,c   Pinto, Alexander R ^a   Rosenthal, Nadia A ^a  

^a JACKSON LABORATORY   (United States)

^b MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Fibrosis; Inflammation; Innate immunity; Regeneration; Wound healing

Indexed keywords

ADAPTIVE IMMUNITY; CELLULAR IMMUNITY; DEVELOPMENTAL STAGE; HOST RESISTANCE; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INJURY; INNATE IMMUNITY; MAMMAL; NONHUMAN; REGENERATIVE MEDICINE; REVIEW; TISSUE REGENERATION; TISSUE REPAIR; VERTEBRATE; WOUND HEALING; ANIMAL; EVOLUTION; PHYSIOLOGY; REGENERATION;

ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; IMMUNE SYSTEM; IMMUNITY, CELLULAR; IMMUNITY, INNATE; REGENERATION; WOUND HEALING;

EID: 84995551114     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2016.08.008     Document Type: Review

References (100)

1. [1] Vishwakarma, A., Bhise, N.S., Evangelista, M.B., Rouwkema, J., Dokmeci, M.R., Ghaemmaghami, A.M., et al. Engineering immunomodulatory biomaterials to tune the inflammatory response. Trends Biotechnol. 34 (2016), 470–482, 10.1016/j.tibtech.2016.03.009.
2. [2] Lane, S.W., Williams, D.A., Watt, F.M., Modulating the stem cell niche for tissue regeneration. Nat. Biotechnol. 32 (2014), 795–803, 10.1038/nbt.2978.
3. [3] Lin, H., Ouyang, H., Zhu, J., Huang, S., Liu, Z., Chen, S., et al. Lens regeneration using endogenous stem cells with gain of visual function. Nature 531 (2016), 323–328, 10.1038/nature17181.
4. [4] Mele, L., Vitiello, P.P., Tirino, V., Paino, F., De Rosa, A., Liccardo, D., et al. Changing paradigms in cranio-facial regeneration: current and new strategies for the activation of endogenous stem cells. Front. Physiol., 7(62), 2016, 10.3389/fphys.2016.00062.
5. [5] Forbes, S.J., Rosenthal, N., Preparing the ground for tissue regeneration: from mechanism to therapy. Nat. Med. 20 (2014), 857–869, 10.1038/nm.3653.
6. [6] Funk, D.J., Parrillo, J.E., Kumar, A., Sepsis and septic shock: a history. Crit. Care Clin., 25, 2009, 10.1016/j.ccc.2008.12.003 (83–101-viii).
7. [7] Heidland, A., Klassen, A., Rutkowski, P., Bahner, U., The contribution of Rudolf Virchow to the concept of inflammation: what is still of importance?. J. Nephrol. 19:Suppl. (10) (2006), S102–9.
8. [8] Oldstone, M., Viruses, Plagues, and History: Past, Present and Future, Revised Edition. 2010, Oxford University Press, New York, USA, 10.5040/9781474215343.ch-011.
9. [9] Olive, C., Pattern recognition receptors: sentinels in innate immunity and targets of new vaccine adjuvants. Expert Rev. Vaccines 11 (2014), 237–256, 10.1586/erv.11.189.
10. [10] Eming, S.A., Martin, P., Tomic-Canic, M., Wound repair and regeneration: mechanisms, signaling, and translation. Sci. Transl. Med., 6, 2014, 265sr6, 10.1126/scitranslmed.3009337.
11. [11] Gurtner, G.C., Werner, S., Barrandon, Y., Longaker, M.T., Wound repair and regeneration. Nature 453 (2008), 314–321, 10.1038/nature07039.
12. [12] Reinke, J.M., Sorg, H., Wound repair and regeneration. Eur. Surg. Res. 49 (2012), 35–43, 10.1159/000339613.
13. [13] Barron, L., Wynn, T.A., Fibrosis is regulated by Th2 and Th17 responses and by dynamic interactions between fibroblasts and macrophages. Am. J. Physiol. Gastrointest. Liver Physiol. 300 (2011), G723–8, 10.1152/ajpgi.00414.2010.
14. [14] Godwin, J., Kuraitis, D., Rosenthal, N., Extracellular matrix considerations for scar-free repair and regeneration: insights from regenerative diversity among vertebrates. Int. J. Biochem. Cell Biol. 56 (2014), 47–55, 10.1016/j.biocel.2014.10.011.
15. [15] Hartupee, J., Mann, D.L., Role of inflammatory cells in fibroblast activation. J. Mol. Cell. Cardiol. 93 (2016), 143–148, 10.1016/j.yjmcc.2015.11.016.
16. [16] He, W., Dai, C., Key fibrogenic signaling. Curr. Pathobiol. Rep. 3 (2015), 183–192, 10.1007/s40139-015-0077-z.
17. [17] Stempien-Otero, A., Kim, D.-H., Davis, J., Molecular networks underlying myofibroblast fate and fibrosis. J. Mol. Cell. Cardiol. 97 (2016), 153–161, 10.1016/j.yjmcc.2016.05.002.
18. [18] Davis, J., Molkentin, J.D., Myofibroblasts: trust your heart and let fate decide. J. Mol. Cell. Cardiol. 70 (2014), 9–18, 10.1016/j.yjmcc.2013.10.019.
19. [19] Kis, K., Liu, X., Hagood, J.S., Myofibroblast differentiation and survival in fibrotic disease. Expert Rev. Mol. Med., 13, 2011, e27, 10.1017/S1462399411001967.
20. [20] DelaRosa, O., Dalemans, W., Lombardo, E., Toll-like receptors as modulators of mesenchymal stem cells. Front. Immun., 3(182), 2012, 10.3389/fimmu.2012.00182.
21. [21] Denu, R.A., Nemcek, S., Bloom, D.D., Goodrich, A.D., Kim, J., Mosher, D.F., et al. Fibroblasts and mesenchymal stromal/stem cells are phenotypically indistinguishable. Acta Haematol. 136 (2016), 85–97, 10.1159/000445096.
22. [22] Halfon, S., Abramov, N., Grinblat, B., Ginis, I., Markers distinguishing mesenchymal stem cells from fibroblasts are downregulated with passaging. Stem Cells Dev. 20 (2011), 53–66, 10.1089/scd.2010.0040.
23. [23] Rohart, F., Mason, E.A., Matigian, N., Mosbergen, R., Korn, O., Chen, T., et al. A molecular classification of human mesenchymal stromal cells. Peer J., 4, 2016, e1845, 10.7717/peerj.1845.
24. [24] Coulson-Thomas, V.J., Coulson-Thomas, Y.M., Gesteira, T.F., Kao, W.W.Y., Extrinsic and intrinsic mechanisms by which mesenchymal stem cells suppress the immune system. Ocular Surf. 14 (2016), 121–134, 10.1016/j.jtos.2015.11.004.
25. [25] McGettrick, H.M., Butler, L.M., Buckley, C.D., Rainger, G.E., Nash, G.B., Tissue stroma as a regulator of leukocyte recruitment in inflammation. J. Leukoc. Biol. 91 (2012), 385–400, 10.1189/jlb.0911458.
26. [26] Smith, R.S., Smith, T.J., Blieden, T.M., Phipps, R.P., Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. Am. J. Pathol. 151 (1997), 317–322.
27. [27] Wynn, T.A., Chawla, A., Pollard, J.W., Macrophage biology in development, homeostasis and disease. Nature 496 (2013), 445–455, 10.1038/nature12034.
28. [28] Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204 (2007), 1057–1069, 10.1084/jem.20070075.
29. [29] Savill, J., Dransfield, I., Gregory, C., Haslett, C., A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2 (2002), 965–975, 10.1038/nri957.
30. [30] Lee, S., Zhang, J., Heterogeneity of macrophages in injured trigeminal nerves: cytokine/chemokine expressing vs. phagocytic macrophages. Brain Behav. Immun. 26 (2012), 891–903, 10.1016/j.bbi.2012.03.004.
31. [31] Mosser, D.M., Edwards, J.P., Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8 (2008), 958–969, 10.1038/nri2448.
32. [32] Davies, L.C., Taylor, P.R., Tissue-resident macrophages: then and now. Immunology 144 (2015), 541–548, 10.1111/imm.12451.
33. [33] Epelman, S., Lavine, K.J., Randolph, G.J., Origin and functions of tissue macrophages. Immunity 41 (2014), 21–35, 10.1016/j.immuni.2014.06.013.
34. [34] Pinto, A.R., Godwin, J.W., Rosenthal, N.A., Macrophages in cardiac homeostasis, injury responses and progenitor cell mobilisation. Stem Cell Res. 13 (2014), 705–714, 10.1016/j.scr.2014.06.004.
35. [35] Varol, C., Mildner, A., Jung, S., Macrophages: development and tissue specialization. Annu. Rev. Immunol. 33 (2015), 643–675, 10.1146/annurev-immunol-032414-112220.
36. [36] Hoeffel, G., Ginhoux, F., Ontogeny of tissue-resident macrophages. Front. Immun., 6(486), 2015, 10.3389/fimmu.2015.00486.
37. [37] Perdiguero, E.G., Geissmann, F., The development and maintenance of resident macrophages. Nat. Immunol. 17 (2016), 2–8, 10.1038/ni.3341.
38. [38] Bain, C.C., Bravo-Blas, A., Scott, C.L., Gomez Perdiguero, E., Geissmann, F., Henri, S., et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15 (2014), 929–937, 10.1038/ni.2967.
39. [39] Molawi, K., Wolf, Y., Kandalla, P.K., Favret, J., Hagemeyer, N., Frenzel, K., et al. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 211 (2014), 2151–2158, 10.1084/jem.20140639.
40. [40] Cumano, A., Godin, I., Ontogeny of the hematopoietic system. Annu. Rev. Immunol. 25 (2007), 745–785, 10.1146/annurev.immunol.25.022106.141538.
41. [41] Mikkola, H.K.A., Orkin, S.H., The journey of developing hematopoietic stem cells. Development 133 (2006), 3733–3744, 10.1242/dev.02568.
42. [42] Morrison, S.J., Scadden, D.T., The bone marrow niche for haematopoietic stem cells. Nature 505 (2014), 327–334, 10.1038/nature12984.
43. [43] Itou, J., Oishi, I., Kawakami, H., Glass, T.J., Richter, J., Johnson, A., et al. Migration of cardiomyocytes is essential for heart regeneration in zebrafish. Development 139 (2012), 4133–4142, 10.1242/dev.079756.
44. [44] Schroeder, M.A., DiPersio, J.F., Mobilization of hematopoietic stem and leukemia cells. J. Leukoc. Biol. 91 (2012), 47–57, 10.1189/jlb.0210085.
45. [45] Wang, J., Knaut, H., Chemokine signaling in development and disease. Development 141 (2014), 4199–4205, 10.1242/dev.101071.
46. [46] Corona, B.T., Garg, K., Ward, C.L., McDaniel, J.S., Walters, T.J., Rathbone, C.R., Autologous minced muscle grafts: a tissue engineering therapy for the volumetric loss of skeletal muscle. AJP: Cell Physiol. 305 (2013), C761–C775, 10.1152/ajpcell.00189.2013.
47. [47] Ferguson, M.W.J., O'Kane, S., Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. Philos. Trans. R. Soc. B: Biol. Sci. 359 (2004), 839–850, 10.1098/rstb.2004.1475.
48. [48] Kishi, K., Okabe, K., Shimizu, R., Kubota, Y., Fetal skin possesses the ability to regenerate completely: complete regeneration of skin. Keio J. Med. 61 (2012), 101–108, 10.2302/kjm.2011-0002-IR.
49. [49] Leavitt, T., Hu, M.S., Marshall, C.D., Barnes, L.A., Lorenz, H.P., Longaker, M.T., Scarless wound healing: finding the right cells and signals. Cell Tissue Res., 2016, 1–11, 10.1007/s00441-016-2424-8.
50. [50] Rolfe, K.J., Grobbelaar, A.O., A review of fetal scarless healing. ISRN Dermatol. 2012 (2012), 1–9, 10.5402/2012/698034.
51. [51] Porrello, E.R., Mahmoud, A.I., Simpson, E., Hill, J.A., Richardson, J.A., Olson, E.N., et al. Transient regenerative potential of the neonatal mouse heart. Science 331 (2011), 1078–1080, 10.1126/science.1200708.
52. [52] Sattler, S., Rosenthal, N., The neonate versus adult mammalian immune system in cardiac repair and regeneration. Biochim. Biophys. Acta 1863 (2016), 1813–1821, 10.1016/j.bbamcr.2016.01.011.
53. [53] Aurora, A.B., Porrello, E.R., Tan, W., Mahmoud, A.I., Hill, J.A., Bassel-Duby, R., et al. Macrophages are required for neonatal heart regeneration. J. Clin. Invest. 124 (2014), 1382–1392, 10.1172/JCI72181.
54. [54] Pinto, A.R., Godwin, J.W., Chandran, A., Hersey, L., Ilinykh, A., Debuque, R., et al. Age-related changes in tissue macrophages precede cardiac functional impairment. Aging (Albany, NY). 6 (2014), 399–413.
55. [55] Thomas, J.A., Pope, C., Wojtacha, D., Robson, A.J., Gordon-Walker, T.T., Hartland, S., et al. Macrophage therapy for murine liver fibrosis recruits host effector cells improving fibrosis, regeneration, and function. Hepatology 53 (2011), 2003–2015, 10.1002/hep.24315.
56. [56] Moore, J.K., Mackinnon, A.C., Wojtacha, D., Pope, C., Fraser, A.R., Burgoyne, P., et al. Phenotypic and functional characterization of macrophages with therapeutic potential generated from human cirrhotic monocytes in a cohort study. Cytotherapy 17 (2015), 1604–1616, 10.1016/j.jcyt.2015.07.016.
57. [57] Ramachandran, P., Pellicoro, A., Vernon, M.A., Boulter, L., Aucott, R.L., Ali, A., et al. Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E3186–95, 10.1073/pnas.1119964109.
58. [58] Tsonis, P.A., Madhavan, M., Tancous, E.E., Del Rio-Tsonis, K., A newt's eye view of lens regeneration. Int. J. Dev. Biol. 48 (2004), 975–980, 10.1387/ijdb.041867pt.
59. [59] Carlson, B.M., Principles of Regenerative Biology. 2007, Academic Press, Burlington, 10.1016/B978-012369439-3/50003-9.
60. [60] Godwin, J., The promise of perfect adult tissue repair and regeneration in mammals: learning from regenerative amphibians and fish. Bioessays 36 (2014), 861–871, 10.1002/bies.201300144.
61. [61] Stocum, D., Regenerative Biology and Medicine. 2nd ed., 2012, Academic press, San Diego.
62. [62] Godwin, J.W., Rosenthal, N., Scar-free wound healing and regeneration in amphibians: immunological influences on regenerative success. Differentiation 87 (2014), 66–75, 10.1016/j.diff.2014.02.002.
63. [63] Mescher, A.L., Neff, A.W., King, M.W., Inflammation and immunity in organ regeneration. Dev. Comp. Immunol., 2016, 10.1016/j.dci.2016.02.015.
64. [64] Godwin, J.W., Pinto, A.R., Rosenthal, N.A., Macrophages are required for adult salamander limb regeneration. Proc. Natl. Acad. Sci. 110 (2013), 9415–9420, 10.1073/pnas.1300290110.
65. [65] Satoh, A., Hirata, A., Makanae, A., Collagen reconstitution is inversely correlated with induction of limb regeneration in ambystoma mexicanum. Zool. Sci. 29 (2012), 191–197, 10.2108/zsj.29.191.
66. [66] Lévesque, M., Villiard, É., Roy, S., Skin wound healing in axolotls: a scarless process. J. Exp. Zool. 314 B (2010), 684–697, 10.1002/jez.b.21371.
67. [67] Petrie, T.A., Strand, N.S., Yang, C.T., Rabinowitz, J.S., Moon, R.T., Macrophages modulate adult zebrafish tail fin regeneration. Development, 142, 2015, 10.1242/dev.120642 (406-406).
68. [68] Lucas, T., Waisman, A., Ranjan, R., Roes, J., Krieg, T., Muller, W., et al. Differential roles of macrophages in diverse phases of skin repair. J. Immunol. 184 (2010), 3964–3977, 10.4049/jimmunol.0903356.
69. [69] Banaei-Bouchareb, L., Gouon-Evans, V., Samara-Boustani, D., Castellotti, M.C., Czernichow, P., Pollard, J.W., et al. Insulin cell mass is altered in Csf1op/Csf1op macrophage-deficient mice. J. Leukoc. Biol. 76 (2004), 359–367, 10.1189/jlb.1103591.
70. [70] Nucera, S., Biziato, D., De Palma, M., The interplay between macrophages and angiogenesis in development, tissue injury and regeneration. Int. J. Dev. Biol. 55 (2011), 495–503, 10.1387/ijdb.103227sn.
71. [71] Rae, F., Woods, K., Sasmono, T., Campanale, N., Taylor, D., Ovchinnikov, D.A., et al. Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter. Dev. Biol. 308 (2007), 232–246, 10.1016/j.ydbio.2007.05.027.
72. [72] Eguchi, G., Itoh, Y., Regeneration of the lens as a phenomenon of cellular transdifferentiation: regulability of the differentiated state of the vertebrate pigment epithelial cell. Trans. Ophthalmol. Soc. U.K. 102:3 (1982), 380–384.
73. [73] Sousounis, K., Michel, C.S., Bruckskotten, M., Maki, N., Borchardt, T., Braun, T., et al. A microarray analysis of gene expression patterns during early phases of newt lens regeneration. Mol. Vis. 19 (2013), 135–145.
74. [74] Kanao, T., Miyachi, Y., Lymphangiogenesis promotes lens destruction and subsequent lens regeneration in the newt eyeball, and both processes can be accelerated by transplantation of dendritic cells. Dev. Biol. 290 (2006), 118–124, 10.1016/j.ydbio.2005.11.017.
75. [75] Godwin, J.W., Brockes, J.P., Regeneration, tissue injury and the immune response. J. Anat. 209 (2006), 423–432, 10.1111/j.1469-7580.2006.00626.x.
76. [76] Fahmy, G.H., Sicard, R.E., A role for effectors of cellular immunity in epimorphic regeneration of amphibian limbs. In Vivo 16 (2002), 179–184.
77. [77] Fukazawa, T., Naora, Y., Kunieda, T., Kubo, T., Suppression of the immune response potentiates tadpole tail regeneration during the refractory period. Development 136 (2009), 2323–2327, 10.1242/dev.033985.
78. [78] Mescher, A.L., Neff, A.W., Limb regeneration in amphibians: immunological considerations. Sci. World J. 6 (2006), 1–11, 10.1100/tsw.2006.323.
79. [79] Robert, J., Ohta, Y., Comparative and developmental study of the immune system in Xenopus. Dev. Dyn. 238 (2009), 1249–1270, 10.1002/dvdy.21891.
80. [80] Cooper, M.D., Alder, M.N., The evolution of adaptive immune systems. Cell 124 (2006), 815–822, 10.1016/j.cell.2006.02.001.
81. [81] Cotter, J.D., Storfer, A., Page, R.B., Beachy, C.K., Voss, S.R., Transcriptional response of Mexican axolotls to Ambystoma tigrinum virus (ATV) infection. BMC Genomics, 9, 2008, 493, 10.1186/1471-2164-9-493.
82. [82] Mescher, A.L., Wolf, W.L., Ashley Moseman, E., Hartman, B., Harrison, C., Nguyen, E., et al. Cells of cutaneous immunity in Xenopus: studies during larval development and limb regeneration. Dev. Comp. Immunol. 31 (2007), 383–393, 10.1016/j.dci.2006.07.001.
83. [83] Heydemann, A., The super super-healing MRL mouse strain. Front. Biol. 7 (2012), 522–538, 10.1007/s11515-012-1192-4.
84. [84] Blankenhorn, E.P., Bryan, G., Kossenkov, A.V., Clark, L.D., Zhang, X.-M., Chang, C., et al. Genetic loci that regulate healing and regeneration in LG/J and SM/J mice. Mamm. Genome 20 (2009), 720–733, 10.1007/s00335-009-9216-3.
85. [85] Cheverud, J.M., Lawson, H.A., Bouckaert, K., Kossenkov, A.V., Showe, L.C., Cort, L., et al. Fine-mapping quantitative trait loci affecting murine external ear tissue regeneration in the LG/J by SM/J advanced intercross line. Heredity (Edinb.) 112 (2014), 508–518, 10.1038/hdy.2013.133.
86. [86] Ito, M.R., Ono, M., Itoh, J., Nose, M., Bone marrow cell transfer of autoimmune diseases in a MRL strain of mice with a deficit in functional Fas ligand: dissociation of arteritis from glomerulonephritis. Pathol. Int. 53 (2003), 518–524.
87. [87] Kench, J.A., Russell, D.M., Fadok, V.A., Young, S.K., Worthen, G.S., Jones-Carson, J., et al. Aberrant wound healing and TGF-beta production in the autoimmune-prone MRL/+ mouse. Clin. Immunol. 92 (1999), 300–310, 10.1006/clim.1999.4754.
88. [88] Omura, T., Omura, K., Tedeschi, A., Riva, P., Painter, M.W., Rojas, L., et al. Robust axonal regeneration occurs in the injured CAST/Ei mouse CNS. Neuron, 90, 2016, 662, 10.1016/j.neuron.2016.04.025.
89. [89] Aleman-Muench, G.R., Soldevila, G., When versatility matters: activins/inhibins as key regulators of immunity. Immunol. Cell Biol. 90 (2012), 137–148, 10.1038/icb.2011.32.
90. [90] Gallego-Colon, E., Sampson, R.D., Sattler, S., Schneider, M.D., Rosenthal, N., Tonkin, J., Cardiac-restricted IGF-1Ea overexpression reduces the early accumulation of inflammatory myeloid cells and mediates expression of extracellular matrix remodelling genes after myocardial infarction. Mediators Inflamm. 2015 (2015), 484357–484410, 10.1155/2015/484357.
91. [91] Bilbao, D., Luciani, L., Johannesson, B., Piszczek, A., Rosenthal, N., Insulin-like growth factor-1 stimulates regulatory T cells and suppresses autoimmune disease. EMBO Mol. Med. 6 (2014), 1423–1435, 10.15252/emmm.201303376.
92. [92] Knapp, D., Schulz, H., Rascón, C.A., Volkmer, M., Scholz, J., Nacu, E., et al. Comparative transcriptional profiling of the axolotl limb identifies a tripartite regeneration-specific gene program. PLoS One, 8, 2013, e61352, 10.1371/journal.pone.0061352.
93. [93] Monaghan, J.R., Athippozhy, A., Seifert, A.W., Putta, S., Stromberg, A.J., Maden, M., et al. Gene expression patterns specific to the regenerating limb of the Mexican axolotl. Biol. Open 1 (2012), 937–948, 10.1242/bio.20121594.
94. [94] Monaghan, J.R., Epp, L.G., Putta, S., Page, R.B., Walker, J.A., Beachy, C.K., et al. Microarray and cDNA sequence analysis of transcription during nerve-dependent limb regeneration. BMC Biol., 7, 2009, 1, 10.1186/1741-7007-7-1.
95. [95] Stewart, R., Rascón, C.A., Tian, S., Nie, J., Barry, C., Chu, L.-F., et al. Comparative RNA-seq analysis in the unsequenced axolotl: the oncogene burst highlights early gene expression in the blastema. PLoS Comput. Biol., 9, 2013, e1002936, 10.1371/journal.pcbi.1002936.
96. [96] Voss, S.R., Palumbo, A., Nagarajan, R., Gardiner, D.M., Muneoka, K., Stromberg, A.J., et al. Gene expression during the first 28 days of axolotl limb regeneration I: Experimental design and global analysis of gene expression. Regeneration (Oxf.) 2 (2015), 120–136, 10.1002/reg2.37.
97. [97] Wu, C.-H., Tsai, M.-H., Ho, C.-C., Chen, C.-Y., Lee, H.-S., De novo transcriptome sequencing of axolotl blastema for identification of differentially expressed genes during limb regeneration. BMC Genomics, 14, 2013, 434, 10.1186/1471-2164-14-434.
98. [98] Sicard, R.E., Differential inflammatory and immunological responses in tissue regeneration and repair. Ann. N.Y. Acad. Sci. 961 (2002), 368–371, 10.1111/j.1749-6632.2002.tb03126.x.
99. [99] Schilling, J.A., Joel, W., Shurley, H.M., Wound healing: a comparative study of the histochemical changes in granulation tissue contained in stainless steel wire mesh and polyvinyl sponge cylinders. Surgery 46 (1959), 702–710.
100. [100] Hu, W., Pasare, C., Location, location, location: tissue-specific regulation of immune responses. J. Leukoc. Biol. 94 (2013), 409–421, 10.1189/jlb.0413207.