Genetic lineage tracing of Sca-1+ cells reveals endothelial but not myogenic contribution to the murine heart

Circulation

Volumn 138, Issue 25, 2018, Pages 2931-2939

  Vagnozzi, Ronald J ^a   Sargent, Michelle A ^a   Lin, Suh Chin J ^a   Palpant, Nathan J ^c   Murry, Charles E ^d   Molkentin, Jeffery D ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Cell lineage; Endothelial cells; Myocardial infarction; Regeneration; Stem cells

Indexed keywords

CRE RECOMBINASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET ENDOTHELIAL CELL ADHESION MOLECULE 1; STEM CELL ANTIGEN 1; TAMOXIFEN; LY ANTIGEN; LY6A PROTEIN, MOUSE; MEMBRANE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CELL LINEAGE; CELL RENEWAL; CONFOCAL MICROSCOPY; CORONARY ARTERY LIGATION; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENOTYPE; HEART; HEART INFARCTION; HEART INJURY; HEMATOPOIETIC STEM CELL; HETEROZYGOSITY; IMMUNOHISTOCHEMISTRY; ISOTOPE TRACING; MOUSE; NONHUMAN; POSTNATAL GROWTH; PRIORITY JOURNAL; VASCULAR REMODELING; VASCULARIZATION; ADULT STEM CELL; AGING; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CORONARY BLOOD VESSEL; GENETICS; HUMAN; METABOLISM; MUSCLE DEVELOPMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; SURGERY; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

ADULT STEM CELLS; AGING; ANIMALS; ANTIGENS, LY; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; HEART; HUMANS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; MUSCLE DEVELOPMENT; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC;

EID: 85057126786     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.118.035210     Document Type: Article

References (37)

1. Becher UM, Tiyerili V, Skowasch D, Nickenig G, Werner N. Personalized cardiac regeneration by stem cells: hype or hope? EPMA J. 2011;2:119-130. doi: 10.1007/s13167-011-0068-z
2. Nguyen PK, Rhee JW, Wu JC. Adult stem cell therapy and heart failure, 2000 to 2016: a systematic review. JAMA Cardiol. 2016;1:831-841. doi: 10.1001/jamacardio.2016.2225
3. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, Wu TD, Guerquin-Kern JL, Lechene CP, Lee RT. Mammalian heart renewal by pre-existing cardiomyocytes. Nature. 2013;493:433-436. doi: 10.1038/nature11682
4. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98-102. doi: 10.1126/science.1164680
5. Bergmann O, Zdunek S, Felker A, Salehpour M, Alkass K, Bernard S, Sjostrom SL, Szewczykowska M, Jackowska T, Dos Remedios C, Malm T, Andra M, Jashari R, Nyengaard JR, Possnert G, Jovinge S, Druid H, Frisen J. Dynamics of cell generation and turnover in the human heart. Cell. 2015;161:1566-1575. doi: 10.1016/j.cell.2015.05.026
6. Eschenhagen T, Bolli R, Braun T, Field LJ, Fleischmann BK, Frisen J, Giacca M, Hare JM, Houser S, Lee RT, Marban E, Martin JF, Molkentin JD, Murry CE, Riley PR, Ruiz-Lozano P, Sadek HA, Sussman MA, Hill JA. Cardiomyocyte regeneration: a consensus statement. Circulation. 2017;136:680-686. doi: 10.1161/CIRCULATIONAHA.117.029343
7. Cai CL, Molkentin JD. The elusive progenitor cell in cardiac regeneration: slip slidin' away. Circ Res. 2017;120:400-406. doi: 10.1161/CIRCRESAHA. 116.309710
8. Leri A, Kajstura J, Anversa P. Role of cardiac stem cells in cardiac pathophysiology: a paradigm shift in human myocardial biology. Circ Res. 2011;109:941-961. doi: 10.1161/CIRCRESAHA.111.243154
9. 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.
10. Ellison GM, Vicinanza C, Smith AJ, Aquila I, Leone A, Waring CD, Henning BJ, Stirparo GG, Papait R, Scarfo M, Agosti V, Viglietto G, Condorelli G, Indolfi C, Ottolenghi S, Torella D, Nadal-Ginard B. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell. 2013;154:827-842. doi: 10.1016/j.cell.2013.07.039
11. Liang SX, Tan TY, Gaudry L, Chong B. Differentiation and migration of Sca1+/CD31- cardiac side population cells in a murine myocardial ischemic model. Int J Cardiol. 2010;138:40-49. doi: 10.1016/j.ijcard.2008.08.032
12. Oh H, Chi X, Bradfute SB, Mishina Y, Pocius J, Michael LH, Behringer RR, Schwartz RJ, Entman ML, Schneider MD. Cardiac muscle plasticity in adult and embryo by heart-derived progenitor cells. Ann N Y Acad Sci. 2004;1015:182-189. doi: 10.1196/annals.1302.015
13. van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin SC, Middleton RC, Marban E, Molkentin JD. c-Kit+ cells minimally contribute cardiomyocytes to the heart. Nature. 2014;509:337-341. doi: 10.1038/nature13309
14. Hatzistergos KE, Takeuchi LM, Saur D, Seidler B, Dymecki SM, Mai JJ, White IA, Balkan W, Kanashiro-Takeuchi RM, Schally AV, Hare JM. cKit+ cardiac progenitors of neural crest origin. Proc Natl Acad Sci U S A. 2015;112:13051-13056. doi: 10.1073/pnas.1517201112
15. Sultana N, Zhang L, Yan J, Chen J, Cai W, Razzaque S, Jeong D, Sheng W, Bu L, Xu M, Huang GY, Hajjar RJ, Zhou B, Moon A, Cai CL. Resident c-kit(+) cells in the heart are not cardiac stem cells. Nat Commun. 2015;6:8701. doi: 10.1038/ncomms9701
16. Liu Q, Yang R, Huang X, Zhang H, He L, Zhang L, Tian X, Nie Y, Hu S, Yan Y, Zhang L, Qiao Z, Wang QD, Lui KO, Zhou B. Genetic lineage tracing identifies in situ Kit-expressing cardiomyocytes. Cell Res. 2016;26:119-130. doi: 10.1038/cr.2015.143
17. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A. 2003;100:12313-12318. doi: 10.1073/pnas.2132126100
18. Wang X, Hu Q, Nakamura Y, Lee J, Zhang G, From AH, Zhang J. The role of the sca-1+/CD31- cardiac progenitor cell population in postinfarction left ventricular remodeling. Stem Cells. 2006;24:1779-1788. doi: 10.1634/stemcells.2005-0386
19. Noseda M, Harada M, McSweeney S, Leja T, Belian E, Stuckey DJ, Abreu Paiva MS, Habib J, Macaulay I, de Smith AJ, al-Beidh F, Sampson R, Lumbers RT, Rao P, Harding SE, Blakemore AI, Jacobsen SE, Barahona M, Schneider MD. PDGFRα demarcates the cardiogenic clonogenic Sca1+ stem/progenitor cell in adult murine myocardium. Nat Commun. 2015;6:6930. doi: 10.1038/ncomms7930
20. Uchida S, De Gaspari P, Kostin S, Jenniches K, Kilic A, Izumiya Y, Shiojima I, Grosse Kreymborg K, Renz H, Walsh K, Braun T. Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Reports. 2013;1:397-410. doi: 10.1016/j.stemcr.2013.09.004
21. Kaiser RA, Bueno OF, Lips DJ, Doevendans PA, Jones F, Kimball TF, Molkentin JD. Targeted inhibition of p38 mitogen-activated protein kinase antagonizes cardiac injury and cell death following ischemia-reperfusion in vivo. J Biol Chem. 2004;279:15524-15530. doi: 10.1074/jbc.M313717200
22. Pinto AR, Ilinykh A, Ivey MJ, Kuwabara JT, D'Antoni ML, Debuque R, Chandran A, Wang L, Arora K, Rosenthal NA, Tallquist MD. Revisiting cardiac cellular composition. Circ Res. 2016;118:400-409. doi: 10.1161/CIRCRESAHA.115.307778
23. Schwanekamp JA, Lorts A, Vagnozzi RJ, Vanhoutte D, Molkentin JD. Deletion of periostin protects against atherosclerosis in mice by altering inflammation and extracellular matrix remodeling. Arterioscler Thromb Vasc Biol. 2016;36:60-68. doi: 10.1161/ATVBAHA.115.306397
24. Bergmann O, Zdunek S, Alkass K, Druid H, Bernard S, Frisen J. Identification of cardiomyocyte nuclei and assessment of ploidy for the analysis of cell turnover. Exp Cell Res. 2011;317:188-194. doi: 10.1016/j.yexcr.2010.08.017
25. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature. 2003;425:968-973. doi: 10.1038/nature02069
26. Petersen BE, Grossbard B, Hatch H, Pi L, Deng J, Scott EW. Mouse A6- positive hepatic oval cells also express several hematopoietic stem cell markers. Hepatology. 2003;37:632-640. doi: 10.1053/jhep.2003.50104
27. van de Rijn M, Heimfeld S, Spangrude GJ, Weissman IL. Mouse hematopoietic stem-cell antigen Sca-1 is a member of the Ly-6 antigen family. Proc Natl Acad Sci U S A. 1989;86:4634-4638.
28. Dekel B, Zangi L, Shezen E, Reich-Zeliger S, Eventov-Friedman S, Katchman H, Jacob-Hirsch J, Amariglio N, Rechavi G, Margalit R, Reisner Y. Isolation and characterization of nontubular sca-1+lin- multipotent stem/progenitor cells from adult mouse kidney. J Am Soc Nephrol. 2006;17:3300-3314. doi: 10.1681/ASN.2005020195
29. Trevisan M, Iscove NN. Phenotypic analysis of murine long-term hemopoietic reconstituting cells quantitated competitively in vivo and comparison with more advanced colony-forming progeny. J Exp Med. 1995;181:93-103.
30. Holmes C, Stanford WL. Concise review: stem cell antigen-1: expression, function, and enigma. Stem Cells. 2007;25:1339-1347. doi: 10.1634/stemcells.2006-0644
31. Stanford WL, Haque S, Alexander R, Liu X, Latour AM, Snodgrass HR, Koller BH, Flood PM. Altered proliferative response by T lymphocytes of Ly-6A (Sca-1) null mice. J Exp Med. 1997;186:705-717.
32. Ito CY, Li CY, Bernstein A, Dick JE, Stanford WL. Hematopoietic stem cell and progenitor defects in Sca-1/Ly-6A-null mice. Blood. 2003;101:517-523. doi: 10.1182/blood-2002-06-1918
33. Lee SH, Wolf PL, Escudero R, Deutsch R, Jamieson SW, Thistlethwaite PA. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med. 2000;342:626-633. doi: 10.1056/NEJM200003023420904
34. Shiojima I, Sato K, Izumiya Y, Schiekofer S, Ito M, Liao R, Colucci WS, Walsh K. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005;115:2108-2118. doi: 10.1172/JCI24682
35. Lee PY, Wang JX, Parisini E, Dascher CC, Nigrovic PA. Ly6 family proteins in neutrophil biology. J Leukoc Biol. 2013;94:585-594. doi: 10.1189/jlb.0113014
36. Loughner CL, Bruford EA, McAndrews MS, Delp EE, Swamynathan S, Swamynathan SK. Organization, evolution and functions of the human and mouse Ly6/uPAR family genes. Hum Genomics. 2016;10:10. doi: 10.1186/s40246-016-0074-2
37. Li Y, He L, Huang X, Bhaloo SI, Zhao H, Zhang S, Pu W, Tian X, Li Y, Liu Q, Yu W, Zhang L, Liu X, Liu K, Tang J, Zhang H, Cai D, Ralf AH, Xu Q, Lui KO, Zhou B. Genetic lineage tracing of non-myocyte population by dual recombinases [published online ahead of print April 26, 2018]. Circulation. doi: 10.1161/CIRCULATIONAHA.118.034250. http://circ.ahajournals. org/content/early/2018/04/25/CIRCULATIONAHA.118.034250.long.