MiR-128 regulates non-myocyte hyperplasia, deposition of extracellular matrix and Islet1 expression during newt cardiac regeneration

Developmental Biology

Volumn 383, Issue 2, 2013, Pages 253-263

  Witman, Nevin ^a   Heigwer, Jana ^a,c   Thaler, Barbara ^a,d   Lui, Weng Onn ^b   Morrison, Jamie Ian ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d Fachhochschule Campus Wien   (Austria)

Author keywords

Heart; Hyperplasia; Islet1; MiR 128; Newt; Regeneration

Indexed keywords

MICRORNA; MICRORNA 128; PROTEIN ISLET1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC REGENERATION; CELL POPULATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IN SITU HYBRIDIZATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATION; REGULATORY MECHANISM; RNA EXTRACTION; RNA ISOLATION; RNA SEQUENCE; SALAMANDRIDAE;

MAMMALIA; NOTOPHTHALMUS VIRIDESCENS; SALAMANDRIDAE;

EID: 84885853462     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.09.011     Document Type: Article

References (51)

1. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
2. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S., Zupicich J., Alkass K., Buchholz B.A., Druid H., Jovinge S., Frisen J. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
3. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193.
4. Borchardt T., Braun T. Cardiovascular regeneration in non-mammalian model systems: what are the differences between newts and man?. Thromb. Haemost. 2007, 98:311-318.
5. Brade T., Gessert S., Kuhl M., Pandur P. The amphibian second heart field: Xenopus islet-1 is required for cardiovascular development. Dev. Biol. 2007, 311:297-310.
6. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell. 2003, 5:877-889.
7. Chachques J.C. Cellular cardiac regenerative therapy in which patients?. Expert. Rev. Cardiovasc. Ther. 2009, 7:911-919.
8. Chen J.F., Murchison E.P., Tang R., Callis T.E., Tatsuguchi M., Deng Z., Rojas M., Hammond S.M., Schneider M.D., Selzman C.H., Meissner G., Patterson C., Hannon G.J., Wang D.Z. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. US.A 2008, 105:2111-2116.
9. Edgar R., Domrachev M., Lash A.E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
10. Eulalio A., Mano M., Dal Ferro M., Zentilin L., Sinagra G., Zacchigna S., Giacca M. Functional screening identifies miRNAs inducing cardiac regeneration. Nature 2012, 492:376-381.
11. Garcion C., Baltensperger R., Fournier T., Pasquier J., Schnetzer M.A., Gabriel J.P., Metraux J.P. FiRe and microarrays: a fast answer to burning questions. Trends Plant Sci. 2006, 11:320-322.
12. Godlewski J., Nowicki M.O., Bronisz A., Williams S., Otsuki A., Nuovo G., Raychaudhury A., Newton H.B., Chiocca E.A., Lawler S. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res. 2008, 68:9125-9130.
13. Haubner B.J., Adamowicz-Brice M., Khadayate S., Tiefenthaler V., Metzler B., Aitman T., Penninger J.M. Complete cardiac regeneration in a mouse model of myocardial infarction. Aging 2012, 4:966-977.
14. Holman E.C., Campbell L.J., Hines J., Crews C.M. Microarray analysis of microRNA expression during axolotl limb regeneration. PloS One 2012, 7:e41804.
15. Ivey K.N., Muth A., Arnold J., King F.W., Yeh R.F., Fish J.E., Hsiao E.C., Schwartz R.J., Conklin B.R., Bernstein H.S., Srivastava D. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2008, 2:219-229.
16. Kay B.K., Gall J.G. 5S ribosomal RNA genes of the newt Notophthalmus viridescens. Nucleic Acids Res. 1981, 9:6457-6469.
17. Kozomara A., Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39:D152-D157.
18. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
19. Laugwitz K.L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., Lin L.Z., Cai C.L., Lu M.M., Reth M., Platoshyn O., Yuan J.X., Evans S., Chien K.R. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005, 433:647-653.
20. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
21. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
22. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Qyang Y., Bu L., Sasaki M., Martin-Puig S., Sun Y., Evans S.M., Laugwitz K.L., Chien K.R. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
23. Morrison J.I., Borg P., Simon A. Plasticity and recovery of skeletal muscle satellite cells during limb regeneration. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 2010, 24:750-756.
24. Morrison J.I., Loof S., He P., Simon A. Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J. Cell Biol. 2006, 172:433-440.
25. Motohashi N., Alexander M.S., Shimizu-Motohashi Y., Myers J.A., Kawahara G., Kunkel L.M. Regulation of IRS1/Akt insulin signaling by microRNA-128a during myogenesis. J. Cell. Sci. 2013, 126:2678-2691.
26. Nagai T., Komuro I. Gene and cytokine therapy for heart failure: molecular mechanisms in the improvement of cardiac function. Am. J. Physiol. Heart Circ. Physiol. 2012, 303:H501-H512.
27. Nakamura K., Maki N., Trinh A., Trask H.W., Gui J., Tomlinson C.R., Tsonis P.A. miRNAs in newt lens regeneration: specific control of proliferation and evidence for miRNA networking. PloS One 2010, 5:e12058.
28. Nam Y.J., Song K., Luo X., Daniel E., Lambeth K., West K., Hill J.A., Dimaio J.M., Baker L.A., Bassel-Duby R., Olson E.N. Reprogramming of human fibroblasts toward a cardiac fate. Proc. Natl. Acad. Sci. USA 2013, 110:5588-5593.
29. Noetel A., Elfimova N., Altmuller J., Becker C., Becker D., Lahr W., Nurnberg P., Wasmuth H., Teufel A., Buttner R., Dienes H.P., Odenthal M. Next generation sequencing of the Ago2 interacting transcriptome identified chemokine family members as novel targets of neuronal microRNAs in hepatic stellate cells. J. Hepatol. 2013, 58:335-341.
30. Oviedo N.J., Beane W.S. Regeneration: the origin of cancer or a possible cure?. Semin. Cell Dev. Biol. 2009, 20:557-564.
31. Pal S.N., Kofidis T. New cell therapies in cardiology. Expert Rev. Cardiovasc. Ther. 2012, 10:1023-1037.
32. Pandur P., Sirbu I.O., Kuhl S.J., Philipp M., Kuhl M. Islet1-expressing cardiac progenitor cells: a comparison across species. Dev. Genes Evol. 2013, 223:117-129.
33. Piatkowski T., Muhlfeld C., Borchardt T., Braun T. Reconstitution of the myocardium in regenerating newt hearts is preceded by transient deposition of extracellular matrix components. Stem Cells Dev. 2013, 22:1921-1931.
34. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
35. Porrello E.R., Mahmoud A.I., Simpson E., Johnson B.A., Grinsfelder D., Canseco D., Mammen P.P., Rothermel B.A., Olson E.N., Sadek H.A. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. USA 2013, 110:187-192.
36. Poss K.D., Wilson L.G., Keating M.T. Heart regeneration in zebrafish. Science 2002, 298:2188-2190.
37. Qian P., Banerjee A., Wu Z.S., Zhang X., Wang H., Pandey V., Zhang W.J., Lv X.F., Tan S., Lobie P.E., Zhu T. Loss of SNAIL regulated miR-128-2 on chromosome 3p22.3 targets multiple stem cell factors to promote transformation of mammary epithelial cells. Cancer Res. 2012, 72:6036-6050.
38. Roy S., Khanna S., Hussain S.R., Biswas S., Azad A., Rink C., Gnyawali S., Shilo S., Nuovo G.J., Sen C.K. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc. Res. 2009, 82:21-29.
39. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9:671-675.
40. Schuster P., Fontana W., Stadler P.F., Hofacker I.L. From sequences to shapes and back: a case study in RNA secondary structures. Proc. Biol. Sci. 1994, 255:279-284.
41. Sehm T., Sachse C., Frenzel C., Echeverri K. miR-196 is an essential early-stage regulator of tail regeneration, upstream of key spinal cord patterning events. Dev. Biol. 2009, 334:468-480.
42. Senyo S.E., Steinhauser M.L., Pizzimenti C.L., Yang V.K., Cai L., Wang M., Wu T.D., Guerquin-Kern J.L., Lechene C.P., Lee R.T. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493:433-436.
43. Sluijter J.P., van Mil A., van Vliet P., Metz C.H., Liu J., Doevendans P.A., Goumans M.J. MicroRNA-1 and -499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells. Arterioscler. Thromb. Vasc. Biol. 2010, 30:859-868.
44. Thum T., Gross C., Fiedler J., Fischer T., Kissler S., Bussen M., Galuppo P., Just S., Rottbauer W., Frantz S., Castoldi M., Soutschek J., Koteliansky V., Rosenwald A., Basson M.A., Licht J.D., Pena J.T., Rouhanifard S.H., Muckenthaler M.U., Tuschl T., Martin G.R., Bauersachs J., Engelhardt S. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008, 456:980-984.
45. Tsonis P.A., Call M.K., Grogg M.W., Sartor M.A., Taylor R.R., Forge A., Fyffe R., Goldenberg R., Cowper-Sal-lari R., Tomlinson C.R. MicroRNAs and regeneration: Let-7 members as potential regulators of dedifferentiation in lens and inner ear hair cell regeneration of the adult newt. Biochem. Biophys. Res. Commun. 2007, 362:940-945.
46. Vascotto S.G., Beug S., Liversage R.A., Tsilfidis C. Nvbeta-actin and NvGAPDH as normalization factors for gene expression analysis in limb regenerates and cultured blastema cells of the adult newt, Notophthalmus viridescens. Int. J. Dev. Biol. 2005, 49:833-842.
47. Witman N., Murtuza B., Davis B., Arner A., Morrison J.I. Recapitulation of developmental cardiogenesis governs the morphological and functional regeneration of adult newt hearts following injury. Dev. Biol. 2011, 354:67-76.
48. Witten D., Tibshirani R., Gu S.G., Fire A., Lui W.O. Ultra-high throughput sequencing-based small RNA discovery and discrete statistical biomarker analysis in a collection of cervical tumours and matched controls. BMC. Biol. 2010, 8:58.
49. Yin V.P., Lepilina A., Smith A., Poss K.D. Regulation of zebrafish heart regeneration by miR-133. Dev. Biol. 2012, 365:319-327.
50. Zhang Y., Chao T., Li R., Liu W., Chen Y., Yan X., Gong Y., Yin B., Liu W., Qiang B., Zhao J., Yuan J., Peng X. MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J. Mol. Med. 2009, 87:43-51.
51. Zhu Q., Hong A., Sheng N., Zhang X., Matejko A., Jun K.Y., Srivannavit O., Gulari E., Gao X., Zhou X. microParaflo biochip for nucleic acid and protein analysis. Methods Mol. Biol. 2007, 382:287-312.