Reciprocal analyses in zebrafish and medaka reveal that harnessing the immune response promotes cardiac regeneration

eLife

Volumn 6, Issue , 2017, Pages

  Lai, Shih Lei ^a   Marín Juez, Rubén ^a   Moura, Pedro Luís ^a,b   Kuenne, Carsten ^a   Lai, Jason Kuan Han ^a   Tsedeke, Ayele Taddese ^a   Guenther, Stefan ^a   Looso, Mario ^a   Stainier, Didier Y R ^a  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COLD INJURY; CONTROLLED STUDY; GENE EXPRESSION; GENE ONTOLOGY; HEART DISEASE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIPID METABOLISM; NONHUMAN; ORYZIAS; PHAGOCYTOSIS; PRINCIPAL COMPONENT ANALYSIS; REGENERATION; RNA EXTRACTION; STRESS; TISSUE INJURY; ZEBRA FISH; ANIMAL; CARDIAC MUSCLE CELL; CELLULAR IMMUNITY; GENE EXPRESSION PROFILING; HEART INJURY; IMMUNOLOGY; MACROPHAGE; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; GENE EXPRESSION PROFILING; HEART INJURIES; IMMUNITY, CELLULAR; MACROPHAGES; MYOCYTES, CARDIAC; NEUTROPHILS; ORYZIAS; REGENERATION; ZEBRAFISH;

EID: 85023646705     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.25605     Document Type: Article

References (55)

1. Aurora AB, Porrello ER, Tan W, Mahmoud AI, Hill JA, Bassel-Duby R, Sadek HA, Olson EN. 2014. Macrophages are required for neonatal heart regeneration. Journal of Clinical Investigation 124:1382–1392. doi: 10.1172/JCI72181, PMID: 24569380
2. Bednarek D, González-Rosa JM, Guzmán-Martínez G, Gutiérrez-Gutiérrez Ó, Aguado T, Sánchez-Ferrer C, Marques IJ, Galardi-Castilla M, de Diego I, Gómez MJ, Cortés A, Zapata A, Jiménez-Borreguero LJ, Mercader N, Flores I. 2015. Telomerase is essential for Zebrafish Heart Regeneration. Cell Reports 12:1691–1703. doi: 10. 1016/j.celrep.2015.07.064, PMID: 26321646
3. Bennett CM, Kanki JP, Rhodes J, Liu TX, Paw BH, Kieran MW, Langenau DM, Delahaye-Brown A, Zon LI, Fleming MD, Look AT. 2001. Myelopoiesis in the zebrafish, Danio rerio. Blood 98:643–651. doi: 10.1182/blood.V98.3.643, PMID: 11468162
4. Bernut A, Herrmann JL, Kissa K, Dubremetz JF, Gaillard JL, Lutfalla G, Kremer L. 2014. Mycobacterium abscessus cording prevents phagocytosis and promotes abscess formation. PNAS 111:E943–E952. doi: 10.1073/pnas.1321390111, PMID: 24567393
5. Bersell K, Arab S, Haring B, Kühn B. 2009. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 138:257–270. doi: 10.1016/j.cell.2009.04.060, PMID: 19632177
6. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi: 10.1093/bioinformatics/btu170, PMID: 24695404
7. Chablais F, Jazwinska A. 2012. The regenerative capacity of the zebrafish heart is dependent on tgfβ signaling. Development 139:1921–1930. doi: 10.1242/dev.078543, PMID: 22513374
8. Chablais F, Veit J, Rainer G, Jaźwińska A. 2011. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Developmental Biology 11:21. doi: 10.1186/1471-213X-11-21, PMID: 21473762
9. D’Uva G, Aharonov A, Lauriola M, Kain D, Yahalom-Ronen Y, Carvalho S, Weisinger K, Bassat E, Rajchman D, Yifa O, Lysenko M, Konfino T, Hegesh J, Brenner O, Neeman M, Yarden Y, Leor J, Sarig R, Harvey RP, Tzahor E. 2015. ERBB2 triggers mammalian heart regeneration by promoting cardiomyocyte dedifferentiation and proliferation. Nature Cell Biology 17:627–638. doi: 10.1038/ncb3149, PMID: 25848746
10. de Preux Charles AS, Bise T, Baier F, Marro J, Jaźwińska A. 2016a. Distinct effects of inflammation on preconditioning and regeneration of the adult zebrafish heart. Open Biology 6:160102. doi: 10.1098/rsob. 160102, PMID: 27440424
11. de Preux Charles AS, Bise T, Baier F, Sallin P, Jaźwińska A. 2016b. Preconditioning boosts regenerative programmes in the adult zebrafish heart. Open Biology 6:160101. doi: 10.1098/rsob.160101, PMID: 27440423
12. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. doi: 10.1093/bioinformatics/bts635, PMID: 23104 886
13. Ellett F, Pase L, Hayman JW, Andrianopoulos A, Lieschke GJ. 2011. mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117:e49–e56. doi: 10.1182/blood-2010-10-314120, PMID: 21084707
14. Furutani-Seiki M, Wittbrodt J. 2004. Medaka and zebrafish, an evolutionary twin study. Mechanisms of Development 121:629–637. doi: 10.1016/j.mod.2004.05.010, PMID: 15210172
15. Gemberling M, Karra R, Dickson AL, Poss KD. 2015. Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. eLife 4:e05871. doi: 10.7554/eLife.05871, PMID: 25 830562
16. Godwin JW, Pinto AR, Rosenthal NA. 2013. Macrophages are required for adult salamander limb regeneration. PNAS 110:9415–9420. doi: 10.1073/pnas.1300290110, PMID: 23690624
17. Godwin JW, Pinto AR, Rosenthal NA. 2017. Chasing the recipe for a pro-regenerative immune system. Seminars in Cell & Developmental Biology 61:71–79. doi: 10.1016/j.semcdb.2016.08.008, PMID: 27521522
18. González-Rosa JM, Martín V, Peralta M, Torres M, Mercader N. 2011. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 138:1663–1674. doi: 10.1242/dev.060897, PMID: 21429987
19. Goulopoulou S, McCarthy CG, Webb RC. 2016. Toll-like receptors in the vascular system: sensing the Dangers within. Pharmacological Reviews 68:142–167. doi: 10.1124/pr.114.010090, PMID: 26721702
20. Grimes AC, Durán AC, Sans-Coma V, Hami D, Santoro MM, Torres M. 2010. Phylogeny informs ontogeny: a proposed common theme in the arterial pole of the vertebrate heart. Evolution & Development 12:552–567. doi: 10.1111/j.1525-142X.2010.00441.x, PMID: 21040422
21. Grote K, Schütt H, Schieffer B. 2011. Toll-like receptors in angiogenesis. The Scientific World JOURNAL 11:981– 991. doi: 10.1100/tsw.2011.92, PMID: 21516292
22. Han C, Nie Y, Lian H, Liu R, He F, Huang H, Hu S. 2015. Acute inflammation stimulates a regenerative response in the neonatal mouse heart. Cell Research 25:1137–1151. doi: 10.1038/cr.2015.110, PMID: 26358185
23. Heallen T, Morikawa Y, Leach J, Tao G, Willerson JT, Johnson RL, Martin JF. 2013. Hippo signaling impedes adult heart regeneration. Development 140:4683–4690. doi: 10.1242/dev.102798, PMID: 24255096
24. Hu L, Zang MD, Wang HX, Li JF, Su LP, Yan M, Li C, Yang QM, Liu BY, Zhu ZG. 2016. Biglycan stimulates VEGF expression in endothelial cells by activating the TLR signaling pathway. Molecular Oncology 10:1473–1484. doi: 10.1016/j.molonc.2016.08.002, PMID: 27590684
25. Huang WC, Yang CC, Chen IH, Liu YM, Chang SJ, Chuang YJ. 2013a. Treatment of glucocorticoids inhibited early immune responses and impaired cardiac repair in adult zebrafish. PLoS One 8:e66613. doi: 10.1371/journal.pone.0066613, PMID: 23805247
26. Huang Y, Harrison MR, Osorio A, Kim J, Baugh A, Duan C, Sucov HM, Lien CL. 2013b. Igf signaling is required for Cardiomyocyte proliferation during Zebrafish Heart Development and Regeneration. PLoS One 8:e67266. doi: 10.1371/journal.pone.0067266, PMID: 23840646
27. Ismail JA, Poppa V, Kemper LE, Scatena M, Giachelli CM, Coffin JD, Murry CE. 2003. Immunohistologic labeling of murine endothelium. Cardiovascular Pathology 12:82–90. doi: 10.1016/S1054-8807(02)00166-7, PMID: 126 84163
28. Ito K, Morioka M, Kimura S, Tasaki M, Inohaya K, Kudo A. 2014. Differential reparative phenotypes between zebrafish and medaka after cardiac injury. Developmental Dynamics 243:1106–1115. doi: 10.1002/dvdy.24154, PMID: 24947076
29. Kikuchi K, Gupta V, Wang J, Holdway JE, Wills AA, Fang Y, Poss KD. 2011. tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development 138:2895–2902. doi: 10. 1242/dev.067041, PMID: 21653610
30. Kikuchi K, Poss KD. 2012. Cardiac regenerative capacity and mechanisms. Annual Review of Cell and Developmental Biology 28:719–741. doi: 10.1146/annurev-cellbio-101011-155739, PMID: 23057748
31. Kim J, Wu Q, Zhang Y, Wiens KM, Huang Y, Rubin N, Shimada H, Handin RI, Chao MY, Tuan TL, Starnes VA, Lien CL. 2010. PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. PNAS 107:17206–17210. doi: 10.1073/pnas.0915016107, PMID: 20858732
32. Kinkel MD, Eames SC, Philipson LH, Prince VE. 2010. Intraperitoneal injection into adult zebrafish. Journal of Visualized Experiments 30:e2126. doi: 10.3791/2126
33. Lavine KJ, Epelman S, Uchida K, Weber KJ, Nichols CG, Schilling JD, Ornitz DM, Randolph GJ, Mann DL. 2014. Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart. PNAS 111:16029–16034. doi: 10.1073/pnas.1406508111, PMID: 25349429
34. Lemanski LF, Fitts EP, Marx BS. 1975. Fine structure of the heart in the Japanese Medaka, Oryzias latipes. Journal of Ultrastructure Research 53:37–65. doi: 10.1016/S0022-5320(75)80085-2, PMID: 171438
35. Li L, Yan B, Shi YQ, Zhang WQ, Wen ZL. 2012. Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. Journal of Biological Chemistry 287:25353–25360. doi: 10. 1074/jbc.M112.349126, PMID: 22573321
36. Liao Y, Smyth GK, Shi W. 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. doi: 10.1093/bioinformatics/btt656, PMID: 24227677
37. Lieschke GJ, Oates AC, Crowhurst MO, Ward AC, Layton JE. 2001. Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish. Blood 98:3087–3096. doi: 10.1182/blood. V98.10.3087, PMID: 11698295
38. Lörchner H, Pöling J, Gajawada P, Hou Y, Polyakova V, Kostin S, Adrian-Segarra JM, Boettger T, Wietelmann A, Warnecke H, Richter M, Kubin T, Braun T. 2015. Myocardial healing requires Reg3β-dependent accumulation of macrophages in the ischemic heart. Nature Medicine 21:353–362. doi: 10.1038/nm.3816, PMID: 25751817
39. Maddox DE, Shibata S, Goldstein IJ. 1982. Stimulated macrophages express a new glycoprotein receptor reactive with Griffonia simplicifolia I-B4 isolectin. PNAS 79:166–170. doi: 10.1073/pnas.79.1.166, PMID: 67 98567
40. Marín-Juez R, Marass M, Gauvrit S, Rossi A, Lai SL, Materna SC, Black BL, Stainier DY. 2016. Fast revascularization of the injured area is essential to support zebrafish heart regeneration. PNAS 113:11237– 11242. doi: 10.1073/pnas.1605431113, PMID: 27647901
41. Meda C, Molla F, De Pizzol M, Regano D, Maione F, Capano S, Locati M, Mantovani A, Latini R, Bussolino F, Giraudo E. 2012. Semaphorin 4A exerts a proangiogenic effect by enhancing vascular endothelial growth factor-A expression in macrophages. The Journal of Immunology 188:4081–4092. doi: 10.4049/jimmunol.1101435, PMID: 22442441
42. Moriyama A, Inohaya K, Maruyama K, Kudo A. 2010. Bef medaka mutant reveals the essential role of c-myb in both primitive and definitive hematopoiesis. Developmental Biology 345:133–143. doi: 10.1016/j.ydbio.2010. 06.031, PMID: 20621080
43. Perez-Llamas C, Lopez-Bigas N. 2011. Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS One 6:e19541. doi: 10.1371/journal.pone.0019541, PMID: 21602921
44. Poss KD, Wilson LG, Keating MT. 2002. Heart regeneration in zebrafish. Science 298:2188–2190. doi: 10.1126/science.1077857, PMID: 12481136
45. Raya A, Koth CM, Büscher D, Kawakami Y, Itoh T, Raya RM, Sternik G, Tsai HJ, Rodríguez-Esteban C, Izpisúa-Belmonte JC. 2003. Activation of notch signaling pathway precedes heart regeneration in zebrafish. PNAS 100 Suppl 1:11889–11895. doi: 10.1073/pnas.1834204100, PMID: 12909711
46. Renshaw SA, Loynes CA, Trushell DM, Elworthy S, Ingham PW, Whyte MK. 2006. A transgenic zebrafish model of neutrophilic inflammation. Blood 108:3976–3978. doi: 10.1182/blood-2006-05-024075, PMID: 16926288
47. Schaafhausen MK, Yang WJ, Centanin L, Wittbrodt J, Bosserhoff A, Fischer A, Schartl M, Meierjohann S. 2013. Tumor angiogenesis is caused by single melanoma cells in a manner dependent on reactive oxygen species and NF-kB. Journal of Cell Science 126:3862–3872. doi: 10.1242/jcs.125021, PMID: 23843609
48. Schnabel K, Wu CC, Kurth T, Weidinger G. 2011. Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS One 6:e18503. doi: 10. 1371/journal.pone.0018503, PMID: 21533269
49. Sorokin SP, Hoyt RF. 1992. Macrophage development: I. rationale for using Griffonia simplicifolia isolectin B4 as a marker for the line. The Anatomical Record 232:520–526. doi: 10.1002/ar.1092320409, PMID: 1372795
50. Sorokin SP, McNelly NA, Hoyt RF. 1994. Early development of macrophages in intact and organ cultured hearts of rat embryos. The Anatomical Record 239:306–314. doi: 10.1002/ar.1092390309, PMID: 7943762
51. Taneda Y, Konno S, Makino S, Morioka M, Fukuda K, Imai Y, Kudo A, Kawakami A. 2010. Epigenetic control of cardiomyocyte production in response to a stress during the medaka heart development. Developmental Biology 340:30–40. doi: 10.1016/j.ydbio.2010.01.014, PMID: 20096279
52. Vivien CJ, Hudson JE, Porrello ER. 2016. Evolution, comparative biology and ontogeny of vertebrate heart regeneration. Npj Regenerative Medicine 1:16012. doi: 10.1038/npjregenmed.2016.12
53. Xin M, Kim Y, Sutherland LB, Murakami M, Qi X, McAnally J, Porrello ER, Mahmoud AI, Tan W, Shelton JM, Richardson JA, Sadek HA, Bassel-Duby R, Olson EN. 2013. Hippo pathway effector yap promotes cardiac regeneration. PNAS 110:13839–13844. doi: 10.1073/pnas.1313192110, PMID: 23918388
54. Zhang R, Han P, Yang H, Ouyang K, Lee D, Lin YF, Ocorr K, Kang G, Chen J, Stainier DY, Yelon D, Chi NC. 2013. In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 498:497–501. doi: 10.1038/nature12322, PMID: 23783515
55. Zhao L, Borikova AL, Ben-Yair R, Guner-Ataman B, MacRae CA, Lee RT, Burns CG, Burns CE. 2014. Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. PNAS 111:1403–1408. doi: 10.1073/pnas.1311705111, PMID: 24474765