Localization of islet-1-positive cells in the healthy and infarcted adult murine heart

Circulation Research

Volumn 110, Issue 10, 2012, Pages 1303-1310

  Weinberger, Florian ^a   Mehrkens, Dennis ^a   Friedrich, Felix W ^a   Stubbendorff, Mandy ^a   Hua, Xiaoqin ^a   Müller, Jana Christina ^a   Schrepfer, Sonja ^a   Evans, Sylvia M ^b   Carrier, Lucie ^a,c   Eschenhagen, Thomas ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c Sorbonne Université   (France)

Author keywords

cardiac progenitor cells; cardiac transcription factors; sinoatrial node

Indexed keywords

ALPHA ACTININ; BETA GALACTOSIDASE; MESSENGER RNA; MYOSIN HEAVY CHAIN; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ISLET 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE INSERTION; GENE LOCUS; GENE TARGETING; HEART ATRIUM SEPTUM; HEART INFARCTION; HEART MUSCLE CELL; HEART RIGHT ATRIUM; HUMAN; ISLET 1 POSITIVE CELL; MOUSE; NONHUMAN; PARASYMPATHETIC NERVE; PRIORITY JOURNAL; PULMONARY VEIN; SENSITIVITY AND SPECIFICITY; SINUS NODE; SMOOTH MUSCLE FIBER; SUPERIOR CAVA VEIN;

AGE FACTORS; ANIMALS; AORTA; BIOLOGICAL MARKERS; CHROMOGENIC COMPOUNDS; GALACTOSIDES; INDOLES; LAC OPERON; LIM-HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIAL INFARCTION; MYOCARDIUM; PULMONARY ARTERY; RNA, MESSENGER; SINOATRIAL NODE; TRANSCRIPTION FACTORS;

EID: 84861100146     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.259630     Document Type: Article

References (33)

1. Velagaleti RS, Pencina MJ, Murabito JM, Wang TJ, Parikh NI, D'Agostino RB, Levy D, Kannel WB, Vasan RS. Long-term trends in the incidence of heart failure after myocardial infarction. Circulation. 2008; 118:2057-2062.
2. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisén J. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98-102.
3. Hsieh PCH, Segers VFM, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nature Med. 2007;13:970-974. (Pubitemid 47222045)
4. Loffredo FS, Steinhauser ML, Gannon J, Lee RT. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell. 2011;8:389-398.
5. Angert D, Berretta RM, Kubo H, Zhang H, Chen X, Wang W, Ogorek B, Barbe M, Houser SR. Repair of the injured adult heart involves new myocytes potentially derived from resident cardiac stem cells. Circ Res. 2011.
6. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal- Ginard B, Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003;114:763-776. (Pubitemid 37186770)
7. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P. Bone marrow stem cells regenerate infarcted myocardium. Pediatr Transplant. 2003;7(Suppl 3):86-88. (Pubitemid 36314227)
8. Matsuura K, Nagai T, Nishigaki N, Oyama T, Nishi J, Wada H, Sano M, Toko H, Akazawa H, Sato T, Nakaya H, Kasanuki H, Komuro I. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem. 2004;279:11384-11391. (Pubitemid 38401637)
9. Bu L, Jiang X, Martin-Puig S, Caron L, Zhu S, Shao Y, Roberts DJ, Huang PL, Domian IJ, Chien KR. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature. 2009;460:113-117.
10. Mignone JL, Murry CE. A repair "kit" for the infarcted heart. Cell Stem Cell. 2011;8:350-352.
11. Karlsson O, Thor S, Norberg T, Ohlsson H, Edlund T. Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature. 1990;344:879-882.
12. Ericson J, Thor S, Edlund T, Jessell TM, Yamada T. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 1992;256:1555-1560.
13. Thor S, Andersson SGE, Tomlinson A, Thomas JB. A LIM-homeodomain combinatorial code for motor- neuron pathway selection system, although expression was also observed in precursors of the. Nature. 1999;397:76-80.
14. Cai C-L, Liang X, Shi Y, Chu P-H, Pfaff SL, 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. (Pubitemid 37527688)
15. Sun Y, Liang X, Najafi N, Cass M, Lin L, Cai C-L, Chen J, Evans SM. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol. 2007;304:286-296. (Pubitemid 46399697)
16. Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, Chen Y, Qyang Y, Bu L, Sasaki M, Martin-Puig S, Sun Y, Evans SM, Laugwitz K-L, Chien KR. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell. 2006;127:1151-1165. (Pubitemid 44895618)
17. Laugwitz K-L, Moretti A, Lam J, Gruber P, Chen Y, Woodard S, Lin L-Z, Cai C-L, Lu MM, Reth M, Platoshyn O, Yuan JX-J, Evans S, Chien KR. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature. 2005;433:647-653. (Pubitemid 40282999)
18. Khattar P, Friedrich FW, Bonne G, Carrier L, Eschenhagen T, Evans SM, Schwartz K, Fiszman MY, Vilquin J-T. Distinction between two populations of islet-1-positive cells in hearts of different murine strains. Stem Cell Dev. 2011;20:1043-1052.
19. Genead R, Danielsson C, Andersson AB, Corbascio M, Franco-Cereceda A, Sylvén C, Grinnemo K-H. Islet-1 cells are cardiac progenitors present during the entire lifespan: from the embryonic stage to adulthood. Stem Cell Dev. 2010;19:1601-1615.
20. Hudson REB. The human conducting-system and its examination. J Clin Pathol. 1963;16:492-498.
21. Mangoni ME, Nargeot J. Properties of the hyperpolarization-activated current (I(f)) in isolated mouse sino-atrial cells. Cardiovasc Res. 2001;52: 51-64. (Pubitemid 32835238)
22. Bollini S, Smart N, Riley PR. Resident cardiac progenitor cells: At the heart of regeneration. J Mol Cell Cardiol. 2010;50:296-303.
23. Koelle GB. The histochemical identification of acetylcholinesterase in cholinergic, adrenergic and sensory neurons. J Pharmacol Exp Ther. 1955;114:167-184.
24. Hoover DB, Ganote CE, Ferguson SM, Blakely RD, Parsons RL. Localization of cholinergic innervation in guinea pig heart by immunohistochemistry for highaffinity choline transporters. Cardiovasc Res. 2004;62:112-121. (Pubitemid 38326817)
25. Avivi C, Goldstein RS. Differential expression of Islet-1 in neural crestderived ganglia: Islet-1 + dorsal root ganglion cells are post-mitotic and Islet-1 + sympathetic ganglion cells are still cycling. Brain Res Dev Brain Res. 1999;115:89-92. (Pubitemid 29288636)
26. Sun Y, Dykes IM, Liang X, Eng SR, Evans SM, Turner EE. A central role for Islet1 in sensory neuron development linking sensory and spinal gene regulatory programs. Nat Neurosci. 2008;11:1283-1293.
27. Rysevaite K, Saburkina I, Pauziene N, Vaitkevicius R, Noujaim SF, Jalife J, Pauza DH. Immunohistochemical characterization of the intrinsic cardiac neural plexus in whole-mount mouse heart preparations. Heart Rhythm. 2011;8:731-738.
28. Mommersteeg MT, Dominguez JN, Wiese C, Norden J, de Gier-de Vries C, Burch JB, Kispert A, Brown NA, Moorman AF, Christoffels VM. The sinus venosus progenitors separate and diversify from the first and second heart fields early in development. Cardiovasc Res. 2010;87:92-101.
29. Witman N, Murtuza B, Davis B, Arner A, Morrison JI. Recapitulation of developmental cardiogenesis governs the morphological and functional regeneration of adult newt hearts following injury. Dev Biol. 2011;354:67-76.
30. Smart N, Bollini S, Dubé KN, Vieira JM, Zhou B, Davidson S, Yellon D, Riegler J, Price AN, Lythgoe MF, Pu WT, Riley PR. De novo cardiomyocytes from within the activated adult heart after injury. Nature. 2011;474:640-644.
31. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DYR, Poss KD. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature. 2010;464:601-605.
32. Kiernan JA. Indigogenic substrates for detection and localization of enzymes. Biotech Histochem. 2007;82:73-103. (Pubitemid 47007379)
33. Gonda DK, Bachmair A, Wünning I, Tobias JW, Lane WS, Varshavsky A. Universality and structure of the N-end rule. J Biol Chem. 1989;264:16700-16712.