SCHOOL OF MEDICINE

Department of Medicine

C.P. Chang Laboratory

Chang Lab Publications

Selected peer-reviewed publications

Epigenetic regulation of cardiac pathophysiology or tissue regeneration

  1. Stankunas K, Hang C, Tsun ZY, Chen H, , Lee NV, Wu J, Shing C, Baylor JH, Shou W, Iruela-Arispe L, Chang CP.  Endocardial Brg1 represses ADAMTS1 proteases to maintain the microenvronment for myocardial morphogenesis.  Dev. Cell 2008; 14(2):298-311.
  2. Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang CP, Zhao Y, Swigut T, Wysocka J.  CHD7 cooperates with PBAF to control multipotent neural crest formation.  Nature 2010 ;463(7283):958-962
  3. Hang C, Yang J, Han P, Cheng HL, Ashley E, Zhou B, Chang CP. Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature 2010; 466(7302): 62-67
  4. Han P, Hang CT, Yang J, Chang CP. Chromatin remodeling in cardiovascular development and physiology, Circulation Research 2011; 108: 378-96
  5. Chang CP and Bruneau B. Epigenetics and cardiovascular development. Annual Review of Physiology 2012; 74:13.1–13.28
  6. Li W, Xiong Y, Shang C, Twu K, Hang C, Yang J, Han P, Tsai FC, Stankunas K, Meyer T, Bernstein D, Pan M, Chang CP. Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. Proc Natl Acad Sci 2013; 110 (5): 1738-43. [CHARGE Syndrome Foundation Highlight]
  7. Xiong Y, Li W, Shang C, Chen RM, Han P, Yang J, Stankunas K, Wu B, Pan MG, Zhou B, Longaker MT, Chang CP. Brg1 governs a positive feedback circuit in the hair follicle for tissue regeneration and repair. Dev Cell 2013; 25(2):169-81. Commentary: Mesa KR and Greco V. Linking Morphogen and Chromatin in the hair follicle. Dev Cell 2013; 25(2):113-14
  8. Frey JL, Brady CA, Jung H, Fuentes DR, Kozak MM, Johnson TM, Lin CY, Lin CJ, Swiderski DL, Vogel H, Bernstein JA, Attié-Bitach T, Chang CP, Wysocka J, Martin DM, Attardi LD. Inappropriate p53 activation during development induces features of CHARGE syndrome. Nature 2014 doi: 10.1038/nature13585
  9. Han P, Li W, Lin CH, Yang J, Chang C, Jin KK, Xu W, Yang J, Lin CY, Lin CJ, Xiong Y, Zhou Bin, Ashley E, Chen V, Chen PS, Quertermous T. Chang CP. A long non-coding RNA protects the heart from pathological hypertrophy.  Nature 2014; 514(7520):102-6

Signaling and transcription regulation in heart development and disease

  1. Chang CP, Neilson JR, Bayle JH, Gestwicki JE, Kuo A, Graef  IA, Crabtree GR.  A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis.  Cell 2004 ;118, 649-663. Cover story. Editorial commentary: Carmeliet P.  Sculpting heart valves with NFAT and VEGF. Cell 2004 118, 532-534.
  2. Arron J, Winslow M, Polleri A, Chang CP, Wu H, Gao X, Neilson J, Chen L, Heit J, Kim S, Yamasaki N, Miyakawa T, Francke U, Graef I, Crabtree G.  NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature 2006 ;441(7093):595-600
  3. Wu H, Kao SC, Barriantos T, Baldwin S, Olson E, Crabtree GR, Zhou, B, Chang CP.  DSCR1 is a transcriptional target of NFATc1 within the endocardium during heart development.  J Biological Chemistry  2007;282(42):30673-9.
  4. Jia Q, McDill BW, Li S, Deng C, Chang CP, Chen F. Smad signaling in the neural crest regulates the cardiac outflow tract remodeling through cell autonomous and non-cell autonomous effects. Developmental Biology  2007; 311(1): 172-84
  5. El-Bizri N,  Guignabert C, Wang L,  Cheng A, Stankunas K, Desai K,  Chang CP, Helms J, Mishina Y,  Rabinovitch M.  SM22alpha-targeted deletion of bone morphogenetic protein receptor 1A in mice impairs cardiac and vascular development, and influences organogenesis.  Development 2008,135 (17):2981-91.
  6. Stankunas K, Shang C, Twu KY, Kao SC, Jekins NA, Copeland N, Sanyal M, Selleri L, Cleary ML, Chang CP.  Pbx/Meis deficiencies demonstrate multigenetic origins of congenital heart disease.  Circulation Research 2008;103:702-709 Cover story.
  7. Chang CP*, Stankunas K, Shang C, Kao SC, Twu KY, Cleary ML.  Pbx1 functions in distinct regulatory networks to pattern the great arteries and cardiac outflow tract. * Corresponding author.  Development 2008;135(21):3577-86.
  8. Zeini M, Hang CT, Lehrer-Graiwer J, Zhou B, Chang CP.  Spatial and temporal regulation of coronary vessel formation by calcineurin/NFAT signaling. Development 2009;136 (19), 3335-3345.
  9.  Wu B, Zhou B, Wang Y, Cheng HL, Hang C, Pu WT, Chang CP, Zhou B. Inducible cardiomyocyte-specific gene disruption directed by the rat Tnnt2 promoter in the mouse. Genesis 2009; 48, 63-72
  10. Stankunas K, Ma G, Kuhnert F, Kuo CJ, Chang CP. VEGF signaling has distinct spatiotemporal roles during heart valve development. Developmental Biology 2010;347(2):325-36.
  11. Lin CY, Lin CJ, Chen CH, Chen RM, Zhou B, Chang CP. The secondary heart field is a new site of calcineurin/Nfatc1 signaling for semilunar valve development. J Mol Cell Cardiology 2012; 52(5): 1096 
  12. Lin CJ, Lin CY, Chen CH, Zhou B, Chang CP. Partitioning of the heart: mechanism of cardiac septation and valve development. Development 2012; 139 (18): 3277-99
  13. Wu B, Zhang Z, Lui W, Chen X, Wang Y, Chamberlain A, Moreno-Rodriquez RA, Markwald RR, O’Rourke RP, Sharp DJ, Zheng D, Lenz J, Baldwin HS, Chang CP, Zhou B. Endocardial Cells Form Coronary Arteries by Angiogenesis through Myocardial to Endocardial VEGF Signaling. Cell 2012; 1083-1096.
  14. Zhang W, Chen H, *Chang CP, *Shou W. Molecular mechanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy. Seminars in Medical Genetics, American Journal of Medical Genetics, 2013 Aug;163(3):144-56] *: corresponding author
  15. Yang J, Zeini M, Lin CY, Lin CJ, Xiong Y, Shang C, Han P, Li W, Quertermous T, Zhou B, Chang CP.  Epicardial calcineurin–NFAT signals through Smad2 to direct coronary smooth muscle cell and arterial wall development. Cardiovascular Research 2014;101(1):120-9
  16. Karpinski SV, Kornyeyev D., El-Bizri N., Budas G, Fan P, Jiang Z, Yang J, Anderson ME, Shryock JC, Chang CP, Belardinelli L, Yao L. Intracellular Na overload causes oxidation of CaMKII and leads to Ca mishandling in isolated ventricular myocytes. J Mol Cell Cardiology 2014; 76: 247-256
  17. Wu SP, Kao CY, Wang L, Creighton C, Yang J, Donti T, Harmancey R, Vasquez HG, Graham B, Bellen   H, Taegtmeyer H, Chang CP, Tsai MJ, and Tsai S. Increased COUP-TFII Expression in Adult Hearts Induces Mitochondrial Dysfunction Resulting in Heart Failure. Nature Comm. 2015 in press

Gene regulation mechanism in general

  1. Chang CP, Shen WF, Rozenfeld S, Lawrence HJ, Largman C, Cleary ML.  Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins.  Genes and Development 1995; 9(6):663-74
  2. Shen WF, Chang CP, Rozenfeld S, Lawrence HJ, Cleary ML, Largman C.  Hox Homeodomain Proteins     Exhibit Selective Complex Stability with Pbx and DNA.”  Nucleic Acids Research, 1996, Vol.24, No. 5, 898
  3. Chang CP, Luciano Brocchieri, Shen WF, Largman C, Cleary ML.  Pbx modulation of Hox homeodomain N- terminal arms establishes a gradient of DNA-binding specificities across the Hox locus.  Molecular and Cellular Biology 1996; 16: 1734-1745
  4. Smith KS, Jacobs Y, Chang CP, Cleary ML.  Chimeric oncoprotein E2a-Pbx1 induces apoptosis of hematopoietic cells by a p53-independent mechanism that is suppressed by Bcl-2.”  Oncogene 1997; 14 (24): 2917-26
  5. Chang CP, De Vivo I, Cleary ML.  The Hox cooperativity motif of chimeric oncoprotein E2a-Pbx1 is   necessary and sufficient for oncogenesis.  Molecular and Cellular Biology 1997; 17(1): 81-88
  6. Chang CP, Jacobs Y, Nakamura T, Jenkins NA, Copeland NG, Cleary ML.  Meis proteins are major In   vivo DNA binding partners for wild-type but not chimeric Pbx proteins.  Molecular and Cellular Biology 1997; 17 (10): 5679-5687.
  7. Derek P, Batchelor A, Chang CP, Cleary ML, and Wolberger, C.  Crystal structure of a HoxB1-Pbx1a heterodimer bound to DNA:  Role of the hexapeptide and a fourth homeodomain helix in complex formation.” Cell 1999; 96, 587-597
  8. Chang CP, McDill BW, Neilson JR, Joist HE, Epstein JA, Crabtree GR, Chen F.  Calcineurin is required in the urinary tract mesenchyme for the development of the pyeloureteral peristaltic machinery.  J Clin Invest  2004;113(7):1051-8.  Editorial commentary: Mendelsohn C.  Functional obstruction: the renal pelvis rules.  J Clin Invest  2004;113(7): 957-959.
  9. Kao SC, Wu H, Xie J, Chang CP, Ranish JA, Graef IA, Crabtree GR.  Calcineurin/NFAT signaling is required for neuregulin-regulated schwann cell differentiation.  Science 2009;323(5914):651-4.
  10. Koss M, Bolze A, Brendolan A, Saggese M, Capellini TD, Bojilova E, Boisson B, Prall OW, Elliott DA, Solloway M, Lenti E, Hidaka C, Chang CP, Mahlaoui N, Harvey RP, Casanova JL, Selleri L. Congenital asplenia in mice and humans with mutations in a Pbx/Nkx2-5/p15 Module. <;Dev Cell 2012; 22(5):913-26
  11. Li W, Lin CY, Shang C, Han P, Xiong Y, Lin CJ, Yang J, Selleri L, Chang CP. Pbx1 activates Fgf10 in the mesenchyme of developing lungs. Genesis 2014; 52(5):399-407

Clinical studies and Others

  1. Sheikh AY, Lin SA, Cao F, Cao YA, van der Bogt KE, Chu P, Chang CP, Contag CH, Robbins RC, Wu JC.  Molecular imaging of bone marrow mononuclear cell homing and engraftment in ischemic myocardium.  Stem Cells  2007;25(10):2677-2684.
  2. Kofidis T, de Bruin JL, Hoyt G, Ho Y, Tanaka M, Yamane T, Lebl DR, Swijnenburg RJ, Chang CP, Quertermous T, Robbins RC.  Myocardial restoration with embryonic stem cell bioartificial tissue transplantation. J Heart Lung Transplant 2005;24(6):737-744.
  3. Kofidis T, de Bruin JL, Hoyt G, Lebl DR, Tanaka M, Yamane T, Chang CP, Robbins RC.  Injectable bioartificial myocardial tissue for large-scale intramural cell transfer and functional recovery of injured heart muscle. J Thorac Cardiovasc Surg. 2004;128(4): 571-8
  4. Pelletier MP, Chang CP, Vagelos R, Robbins RC.  Alternative approach for use of a left ventricular assist device with a thrombosed prosthetic valve.  J Heart Lung Transplant 2002; 21(3):402-404.
  5. Rugolotto M, Chang CP, Hu B, Schnittger I, Liang DH.  Clinical use of cardiac ultrasound performed with a hand-carried device in patients admitted for acute cardiac care.  Am J Cardiol 2002;90(9):1040-1042.
  6. Lieber MR, Chang CP, Gallo M, Gauss G, Gerstein R, Islas A.  The mechanism of V(D)J recombination:  site-specificity, reaction fidelity, and immunologic diversity.  Semin Immunol 1994;6(3):143-153.

Methodology

  1. Chang CP, Chen L, Crabtree GR.  Sonographic staging of the developmental status of mouse embryos in utero.  Genesis 2003;36(1):7-11.
  2. Xiong Y, Zhou B, Chang CP.  Analysis of the endocardial-to-mesenchymal transformation of heart valve development by a collagen gel culture assay.  Methods in Molecular Biology:  Cardiovascular Development 2012; 843:21-8
  3. Hang C, Chang CP. Whole embryo culture for heart development studies. Methods in Molecular Biology:  Cardiovascular Development 2012; 843:3-9
  4. Chang CP. Analysis of the patterning of great arteries with angiography and vascular casting.  Methods in Molecular Biology:  Cardiovascular Development 2012; 843:101-9

Original Research

  1. Wu SP, Kao CY, Wang L, Creighton C, Yang J, Donti T, Harmancey R, Vasquez HG, Graham B, Bellen   H, Taegtmeyer H, Chang CP, Tsai MJ, and Tsai S. Increased COUP-TFII Expression in Adult Hearts Induces Mitochondrial Dysfunction Resulting in Heart Failure. Nature Comm. 2015 in press

 

Reviews & Book Chapters

  1. Han P, Hang CT, Yang J, Chang CP. Chromatin remodeling in cardiovascular development and physiology, Circulation Research 2011; 108: 378-96
  2. Chang CP and Bruneau B. Epigenetics and cardiovascular development. Annual Review of Physiology 2012; 74:13.1–13.28
  3. Lin CJ, Lin CY, Chen CH, Zhou B, Chang CP. Partitioning of the heart: mechanism of cardiac septation and valve development. Development 2012; 139 (18): 3277-99
  4. Zhang W, Chen H, *Chang CP, *Shou W. Molecular mechanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy. Seminars in Medical Genetics, American Journal of Medical Genetics, 2013 Aug;163(3):144-56] *: corresponding author
  5. Xiong Y, Zhou B, Chang CP.  Analysis of the endocardial-to-mesenchymal transformation of heart valve development by a collagen gel culture assay.  Methods in Molecular Biology:  Cardiovascular Development 2012; 843:21-8
  6. Hang C, Chang CP. Whole embryo culture for heart development studies. Methods in Molecular Biology:  Cardiovascular Development 2012; 843:3-9
  7. Chang CP. Analysis of the patterning of great arteries with angiography and vascular casting.  Methods in Molecular Biology:  Cardiovascular Development 2012; 843:101-9
  8. Han P and Chang CP. Myheart hits the core of chromatin. Cell Cycle 2015;14(6):787-8 [Featured Article]
  9. Devaux Y, Zangrando J, Schroen B, Creemers EE, Pedrazzini T, Chang CP, Dorn II GW, Thum T, Heymans S. Long noncoding RNAs in cardiac development and ageing. Nature Reviews Cardiology 2015 Apr 7. doi: 10.1038/nrcardio.2015.55. [Epub ahead of print]
  10. Han P and Chang CP. Long non-coding RNA and Chromatin Remodeling. RNA Bio. 2015 Jul 15:0. [Epub ahead of print]