Single-Cell Sequencing of the Healthy and Diseased Heart Reveals Cytoskeleton-Associated Protein 4 as a New Modulator of Fibroblasts Activation

Circulation

Volumn 138, Issue 2, 2018, Pages 166-180

  Gladka, Monika M ^a   Molenaar, Bas ^a   De Ruiter, Hesther ^a   Van Der Elst, Stefan ^a   Tsui, Hoyee ^a   Versteeg, Danielle ^a   Lacraz, Grègory P A ^a   Huibers, Manon M H ^a   Van Oudenaarden, Alexander ^a   Van Rooij, Eva ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Adult heart; Ckap4; Ischemic injury; Myofibroblast; Single cell sequencing

Indexed keywords

CELL PROTEIN; CYTOSKELETON ASSOCIATED PROTEIN 4; RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CKAP4 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL SPECIFICITY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HEART FIBROBLAST; HEART MUSCLE ISCHEMIA; HEART TISSUE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; LABORATORY AUTOMATION; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN ANALYSIS; PROTEIN TARGETING; RNA SEQUENCE; SINGLE CELL ANALYSIS; TRANSCRIPTOMICS; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CASE CONTROL STUDY; DISEASE MODEL; GENETICS; HEART INFARCTION; METABOLISM; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; MYOFIBROBLAST; PATHOLOGY; PHENOTYPE; PROCEDURES; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CASE-CONTROL STUDIES; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; HUMANS; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOFIBROBLASTS; PHENOTYPE; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS;

EID: 85053370500     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.117.030742     Document Type: Article

References (34)

1. 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.
2. Grun D, van Oudenaarden A. Design and analysis of single-cell sequencing experiments. Cell. 2015;163:799-810. doi: 10.1016/j.cell.2015.10.039.
3. Grun D, Muraro MJ, Boisset JC, Wiebrands K, Lyubimova A, Dharmadhikari G, van den Born M, van Es J, Jansen E, Clevers H, de Koning EJP, van Oudenaarden A. De novo prediction of stem cell identity using single-cell transcriptome data. Cell Stem Cell. 2016;19:266-277. doi: 10.1016/j.stem.2016.05.010.
4. DeLaughter DM, Bick AG, Wakimoto H, McKean D, Gorham JM, Kathiriya IS, Hinson JT, Homsy J, Gray J, Pu W, Bruneau BG, Seidman JG, Seidman CE. Single-cell resolution of temporal gene expression during heart development. Dev Cell. 2016;39:480-490. doi: 10.1016/j.devcel.2016.10.001.
5. Muraro MJ, Dharmadhikari G, Grun D, Groen N, Dielen T, Jansen E, van Gurp L, Engelse MA, Carlotti F, de Koning EJ, van Oudenaarden A. A single- cell transcriptome atlas of the human pancreas. Cell Syst. 2016;3:385. e3-394.e3. doi: 10.1016/j.cels.2016.09.002.
6. Li G, Xu A, Sim S, Priest JR, Tian X, Khan T, Quertermous T, Zhou B, Tsao PS, Quake SR, Wu SM. Transcriptomic profiling maps anatomically patterned subpopulations among single embryonic cardiac cells. Dev Cell. 2016;39:491-507. doi: 10.1016/j.devcel.2016.10.014.
7. Hullinger TG, Montgomery RL, Seto AG, Dickinson BA, Semus HM, Lynch JM, Dalby CM, Robinson K, Stack C, Latimer PA, Hare JM, Olson EN, van Rooij E. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res. 2012;110:71-81. doi: 10.1161/CIRCRESAHA.111.244442.
8. Li H, Durbin R. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics. 2009;25:1754-1760. doi: 10.1093/bioinformatics/btp324.
9. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57. doi: 10.1038/nprot.2008.211.
10. Masson-Pevet M, Jongsma HJ, De Bruijne J. Collagenase- and trypsin-dissociated heart cells: a comparative ultrastructural study. J Mol Cell Cardiol. 1976;8:747-757.
11. Spada F, Fuoco C, Pirro S, Paoluzi S, Castagnoli L, Gargioli C, Cesareni G. Characterization by mass cytometry of different methods for the preparation of muscle mononuclear cells. N Biotechnol. 2016;33(5 Pt A):514-523. doi: 10.1016/j.nbt.2015.12.007.
12. Liu L, Cheung TH, Charville GW, Rando TA. Isolation of skeletal muscle stem cells by fluorescence-activated cell sorting. Nat Protoc. 2015;10:1612-1624. doi: 10.1038/nprot.2015.110.
13. Etchevers H. Primary culture of chick, mouse or human neural crest cells. Nat Protoc. 2011;6:1568-1577. doi: 10.1038/nprot.2011.398.
14. Yuelling LW, Du F, Li P, Muradimova RE, Yang ZJ. Isolation of distinct cell populations from the developing cerebellum by microdissection. J Vis Exp. 2014;91:52034.
15. Chorvat D Jr, Kirchnerova J, Cagalinec M, Smolka J, Mateasik A, Chorvatova A. Spectral unmixing of flavin autofluorescence components in cardiac myocytes. Biophys J. 2005;89:L55-L57. doi: 10.1529/biophysj.105.073866.
16. Gao G, Johansson U, Rundquist I, Ollinger K. Lipofuscin-induced autofluorescence of living neonatal rat cardiomyocytes in culture. Mech Ageing Dev. 1994;73:79-86.
17. Grun D, Lyubimova A, Kester L, Wiebrands K, Basak O, Sasaki N, Clevers H, van Oudenaarden A. Single-cell messenger RNA sequencing reveals rare intestinal cell types. Nature. 2015;525:251-255. doi: 10.1038/nature14966.
18. Frey N, Richardson JA, Olson EN. Calsarcins, a novel family of sarcomeric calcineurin-binding proteins. Proc Natl Acad Sci U S A. 2000;97:14632- 14637. doi: 10.1073/pnas.260501097.
19. Frey N, Barrientos T, Shelton JM, Frank D, Rutten H, Gehring D, Kuhn C, Lutz M, Rothermel B, Bassel-Duby R, Richardson JA, Katus HA, Hill JA, Olson EN. Mice lacking calsarcin-1 are sensitized to calcineurin signaling and show accelerated cardiomyopathy in response to pathological biomechanical stress. Nat Med. 2004;10:1336-1343. doi: 10.1038/nm1132.
20. Tarone G, Balligand JL, Bauersachs J, Clerk A, De Windt L, Heymans S, Hilfiker- Kleiner D, Hirsch E, Iaccarino G, Knoll R, Leite-Moreira AF, Lourenco AP, Mayr M, Thum T, Tocchetti CG. Targeting myocardial remodelling to develop novel therapies for heart failure: a position paper from the Working Group on Myocardial Function of the European Society of Cardiology. Eur J Heart Fail. 2014;16:494-508. doi: 10.1002/ejhf.62.
21. van Berlo JH, Maillet M, Molkentin JD. Signaling effectors underlying pathologic growth and remodeling of the heart. J Clin Invest. 2013;123:37-45. doi: 10.1172/JCI62839.
22. Li L, Fan D, Wang C, Wang JY, Cui XB, Wu D, Zhou Y, Wu LL. Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF- β1 pathways in cardiac fibroblasts. Cardiovasc Res. 2011;91:80-89. doi: 10.1093/cvr/cvr067.
23. Colston JT, de la Rosa SD, Koehler M, Gonzales K, Mestril R, Freeman GL, Bailey SR, Chandrasekar B. Wnt-induced secreted protein-1 is a prohypertrophic and profibrotic growth factor. Am J Physiol Heart Circ Physiol. 2007;293:H1839-H1846. doi: 10.1152/ajpheart.00428.2007.
24. Maqbool A, Spary EJ, Manfield IW, Ruhmann M, Zuliani-Alvarez L, Gamboa-Esteves FO, Porter KE, Drinkhill MJ, Midwood KS, Turner NA. Tenascin C upregulates interleukin-6 expression in human cardiac myofibroblasts via toll-like receptor 4. World J Cardiol. 2016;8:340-350. doi: 10.4330/wjc.v8.i5.340.
25. Kong P, Christia P, Frangogiannis NG. The pathogenesis of cardiac fibrosis. Cell Mol Life Sci. 2014;71:549-574. doi: 10.1007/s00018-013-1349-6.
26. Conrads TP, Tocci GM, Hood BL, Zhang CO, Guo L, Koch KR, Michejda CJ, Veenstra TD, Keay SK. CKAP4/p63 is a receptor for the frizzled-8 protein- related antiproliferative factor from interstitial cystitis patients. J Biol Chem. 2006;281:37836-37843. doi: 10.1074/jbc.M604581200.
27. Chavda B, Ling J, Majernick T, Planey SL. Antiproliferative factor (APF) binds specifically to sites within the cytoskeleton-associated protein 4 (CKAP4) extracellular domain. BMC Biochem. 2017;18:13. doi: 10.1186/s12858-017-0088-y.
28. Chen H, Yang WW, Wen QT, Xu L, Chen M. TGF-beta induces fibroblast activation protein expression; fibroblast activation protein expression increases the proliferation, adhesion, and migration of HO-8910PM [corrected]. Exp Mol Pathol. 2009;87:189-194. doi: 10.1016/j.yexmp.2009.09.001.
29. Hashimshony T, Yanai I. Revealing developmental networks by comparative transcriptomics. Transcription. 2010;1:154-158. doi: 10.4161/trns.1.3.13190.
30. 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.
31. Panther F, Williams T, Ritter O. Inhibition of the calcineurin-NFAT signalling cascade in the treatment of heart failure. Recent Pat Cardiovasc Drug Discov. 2009;4:180-186.
32. Marinov GK, Williams BA, McCue K, Schroth GP, Gertz J, Myers RM, Wold BJ. From single-cell to cell-pool transcriptomes: stochasticity in gene expression and RNA splicing. Genome Res. 2014;24:496-510. doi: 10.1101/gr.161034.113.
33. Kehat I, Molkentin JD. Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation. 2010;122:2727-2735. doi: 10.1161/CIRCULATIONAHA.110.942268.
34. Kimura H, Fumoto K, Shojima K, Nojima S, Osugi Y, Tomihara H, Eguchi H, Shintani Y, Endo H, Inoue M, Doki Y, Okumura M, Morii E, Kikuchi A. CKAP4 is a Dickkopf1 receptor and is involved in tumor progression. J Clin Invest. 2016;126:2689-2705. doi: 10.1172/JCI84658.