Watanabe Pediatric Cardiology Research Laboratory
edited 4-2015
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    • Latest Papers (2016-2017)
    • Publications Sorted by Subject >
      • Applying Biophotonic Tools to Study Cardiac Development
      • HEXIM1 in the Embryonic and Adult Heart and Mammary Gland
      • Lymphatics
      • Cardiac Development
      • NCAM in Heart Development
      • Development of the Ventricular Conduction System
      • Role of Cited2 and HIF1a in Development
      • NCAM and Neural and Lens Development
      • NCAM in the SCN
      • Sea Urchin Cell Surface Molecules
      • Other Miscellaneous Collaborative Studies
    • All Primary Publications
    • Chapters, Reviews, Commentaries
  • People--About Us
    • Michiko Watanabe
    • Yong Qiu Doughman
    • Ganga Karunamuni
    • Leina Lunasco
    • Biophotonics Collaborators >
      • Michael Jenkins
      • Pei Ma
      • Andrew Rollins
    • Other Collaborators
  • Projects
    • Biophotonic tools to study the embryonic heart
    • Ethanol-exposure and cardiac defects
    • PSA-NCAM and Heart Function
    • An athletic heart without exercise
  • Teaching
  • Protocols
    • Immunohistology
    • Preparation of avian embryos for histology
  • Recent Presentations
  • Future presentations
  • Andrew Rollins
Published Peer-Reviewed Primary Journal Articles

1. Bertolini DR, Watanabe M, Turner RS (1981) Protease-insensitive sea urchin embryo cell adhesions become protease sensitive in the presence of azide or cytochalasin B. Journal               of Supramolecular Structure and Cellular Biochemistry 15(4), 327-333.

2. Watanabe M, Bertolini DR, Schnitman DR, Turner RS (1982) Reconstitution of embryo-like structures from sea urchin embryo cells: Distinction between cell-cell and cell-substrate associations. Differentiation 21, 79-85.

 3. Watanabe M, Bertolini DR, Kew D, Turner RS (1982) Changes in the nature of the cell           adhesion of the sea urchin embryo. Developmental Biology 91, 278-285.

4. Rutishauser U, Watanabe M, Silver J, Troy FA, Vimr ER (1985) Specific alteration of neural cell adhesion molecule-mediated cell adhesion by an endoneuraminidase. J Cell Biol 101, 1842-1949.

5. Noble M, Albrechtsen M, Moller C, Lyles J, Bock E, Goridis C, Watanabe M, Rutishauser U (1985) Purified astrocytes express NCAM/D2-CAM-like molecules in vitro. Nature 316, 725-728.

6. Tosney KW, Watanabe M, Landmesser L, Rutishauser U (1986) The distribution of NCAM in the chick hindlimb during axon outgrowth and synaptogenesis. Dev Biol 114, 437-452.

7. Maier CE, Watanabe M, Singer M, McQuarrie IG, Sunshine J, Rutishauser U (1986) Antibodies to a neural cell adhesion molecule delay limb regeneration. Proc Natl Acad Sci USA 83, 8395-8399.

8. Garner J, Watanabe M, Rutishauser U (1986) Rapid axonal transport of the neural cell             adhesion molecule. J Neurosci 6(11), 3242-3249.

9. Palter KB, Watanabe M, Stinson L, Mahowald AP, Craig EA (1986) Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol. Cell Biol. 6(4), 1187-203. PMC3667631.

 10. Watanabe M, Frelinger AL, Rutishauser U, Katar M, Alcala J, Maisel H (1989) NCAM in the differentiation of embryonic lens tissue.  Dev Biol 135, 414-423.

11. Watanabe M, Rutishauser U, Silver J (1991) Mechanisms of formation of the retinal ganglion cell and optic fiber layers. J Neurobiol 22(1), 85-96.

12. Snow DM, Watanabe M, Brittis P, Cohen J, Letourneaux P, Silver J (1991) A chondroitin sulfate proteoglycan may regulate the unidirectionality of retinal ganglion cell outgrowth. Development 113, 1473-1485.

13. Burroughs CL, Watanabe M, Morse D (1991) NCAM expression in the developing chicken heart.  J Mol Cell Cardiol 23, 1411-1422.

14. Watanabe M, Kobayashi H, Yao R, Maisel H (1992) Adhesion and junction molecules in      embryonic and adult lens cell differentiation. Acta Opthalmologica, Scandinavia,               Supplement 205, 46-52.

15. Watanabe M, Timm M, Fallah-Najmabadi H (1992) Cardiac expression of polysialylated         NCAM in the chicken embryo: Correlation with the ventricular conduction system.           Developmental Dynamics 194(2), 128-141.

16. Glass JD, Lee W, Shen H, Watanabe M (1994)  Expression of immunoreactive polysialylated            neural cell adhesion molecule in the suprachiasmatic nucleus. Neuroendocrinology 60, 87-      95.

17. Yin X, Watanabe M, Rutishauser U (1995) Effect of polysialic acid on the behavior of retinal           ganglion cell axons during growth into the optic tract and tectum. Development 121, 3439-3446.

18. Lee W, Watanabe M, Glass JD (1995) Photoperiod affects the expression of neural cell         adhesion molecule and polysialic acid in the hypothalamus of the Siberian hamster. Brain        Res 690, 64-72.

19. Fisher S, Watanabe M (1996) Expression of exogenous protein and analysis of morphogenesis in the developing chicken heart using an adenoviral vector. Cardiovasc Res.31,E86-95.

20. Gerety M, Watanabe M (1997) Polysialylated NCAM expression during mesenchymal          transformation of endocardial cells in the primary atrial septum of the embryonic chicken       heart. Anat Rec 247(1), 71-84.

21. Chuck T, Watanabe M (1997) Differential expression of PSA-NCAM and HNK-1 epitopes in the developing cardiac conduction system of the chick. Developmental Dynamics. 209(2) 182-195.          

22. Shen H, Watanabe M, Tomasiewicz H, Rutishauser U, Magnuson T, Glass JD (1997) Role of neural cell adhesion molecule and polysialic acid in mouse circadian clock function.                        Journal of Neurosciences, 17(13) 5221-5229.

 23. Chuck ET, Freeman DM, Watanabe M (corresponding author), Rosenbaum DS. (1997)      Changing activation sequence in the embryonic chick heart: Implications for the                     development of the His-Purkinje system. Circulation Research 81, 470-476.

 24. Fisher SA, Siwik E, Branellec D, Walsh K, Watanabe M. (1997) Forced expression of the     homeobox protein Gax during a critical period of heart development perturbs               morphogenesis. Development 124, 4405-4413.

 25. Watanabe M, Choudhry A, Berlan M, Singal A, Siwik E, Mohr S, Fisher SA. (1998) Developmental remodeling and shortening of the cardiac outflow tract involves myocyte programmed cell death. Development 125, 3809-3820.

26. Shen H, Glass JD , Seki T, Watanabe M (1999) Ultrastructural distribution of polysialylated neural cell adhesion molecule (PSA-NCAM) in the suprachiasmatic nuclei of the adult mouse. Anat.Rec. 256, 448-457.

27. Glass JD, Shen H, Fedorkova L, Chen L, Tomasiewicz H, Watanabe M (2000) Polysialylated neural cell adhesion molecule modulates photic signaling in the mouse suprachiasmatic nucleus. Neuroscience Letters 280(3), 207-210.

28. Viguié C, Jansen HT, Glass JD, Watanabe M, Lehman MN, Karsch FJ (2001) Potential for NCAM-mediated neuroplasticity within the Gonadotropin-releasing hormone neurosecretory system of the ewe. Endocrinology 142(3), 1317-1324.

29. Shen H, Watanabe M, Tomasiewicz H, Glass JD (2001) Genetic deletions of NCAM and PSA impair circadian function in the mouse. Physiology and Behavior 73, 185-193.

30. Watanabe M, Jafri A, Fisher SA (2001) Apoptosis is required for the proper formation of the ventriculo-arterial connections. Dev. Biol. 240, 274-288.

 31. Rothenberg F, Hitomi M, Fisher SA, Watanabe M (2002) Initiation of apoptosis in the developing avian outflow tract myocardium. Developmental Dynamics 223,469-482.

32. Yin Z, Haynie J, Yang X, Han B, Kiatchoosakun S, Restivo J, Yuan S, Conlon R, Hoit, B, Watanabe M, Yang Y.-C. (2002) Essential role of Cited2, a p300/CBP interaction protein, in heart development and neurulation. PNAS USA 99(16), 10488-10493.

33. Glass JD, Watanabe M, Fedorkova L, Shen H, Tomasiewicz H, Rutishauser U. (2003) Circadian and photic control of polysialylated NCAM expression in the suprachiasmatic nucleus. Neuroscience 117, 203-211.

34. Schaefer KS, Doughman YQ,  Fisher SA, Watanabe M. (2004) Dynamic patterns of apoptosis in the developing chicken heart. Dev Dyn 229(3), 489-499.

 35. Sallee D, Qiu Y, Liu J, Watanabe M, Fisher SA (2004) Fas ligand gene transfer to the embryonic heart induces programmed cell death and outflow tract defects. Dev Biol  267(2), 309-319.

36. Sugishita Y, Watanabe M, Fisher SA (2004a) Role of myocardial hypoxia in the remodeling of the embryonic avian cardiac outflow tract. Dev Biol 267 (2), 294-308.

37. Sugishita Y, Leifer DW, Watanabe M, Agani F, Fisher SA (2004b) Hypoxia-responsive signaling regulates the apoptosis-dependent remodeling of the embryonic avian cardiac outflow tract. Dev Biol 273, 285-296.

38. Rothenberg F, Nikolski VP, Watanabe M, Efimov IR (2004) Electrophysiology and anatomy of embryonic rabbit hearts before and after septation.  Am J Physiol 288 (1), H344-H351. (cover article)

39. Rothenberg F, Watanabe M, Rosenbaum D (2005) Emerging patterns of cardiac conduction in the chick embryo: Waveform analysis with photodiode array based optical imaging. Dev Dyn 233(2), 456-465.

40. Wang, M. Qanungo, S., Crow, M., Watanabe, M., and Nieminen, A.-L. (2005) Apoptosis repressor with caspase recruitment domain is expressed in cancer cells and localizes to nuclei.  FEBS Lett., 579, 2411-2415.

41. Wikenheiser J, Doughman Y-Q, Fisher SA, Watanabe M. (2006) Differential levels of hypoxia in the developing chicken heart. Dev Dyn 235(1), 115-123.

42. Jenkins MW, Rothenberg F, Roy D, Nikolski VP, Hu Z, Watanabe M, Wilson DL, Efimov IR, Rollins A (2006) 4D embryonic cardiography using gated optical coherence tomography. Optics Express 14, 736-748.
          http://www.opticsexpress.org/abstract.cfm?URI=OPEX-14-2-736

43. Barbosky L, Lawrence DK, Karunamuni G, Wikenheiser J, Doughman Y-Q, Visconti R, Burch J, Watanabe M (2006) Apoptosis in the developing mouse outflow tract. Dev Dyn 235(9), 2592-2602.

44. Xu, B, Doughman Y-Q, Turakhia M, Semenza GL, Watanabe M (co-corresponding author), Yang, Y-C (2007) Partial rescue of defects in Cited2-deficient embryos by HIF1-alpha heterozygosity.  Dev Biol 301(1), 130-140. PMCID:PMC24673.

45. Jenkins MW, Patel P, Deng H, Montano M, Watanabe M, Rollins AM (2007) Phenotyping transgenic embryonic murine hearts using optical coherence tomography. Applied Optics 46, 1776-1781.
http://www.opticsinfobase.org/abstract.cfm?URI=ao-46-10-1776

46. Jenkins MW, DC Adler, M Gargesha, R Huber, F Rothenberg, J Belding, M
Watanabe
, DL Wilson, JG Fujimoto and AM Rollins (2007) Ultrahigh-speed
optical coherence tomography imaging and visualization of the
embryonic avian heart using a buffered Fourier Domain Mode Locked
laser.  Optics Express 15, 6251-6267. http://www.opticsinfobase.org/abstract.cfm?URI=oe-15-10-6251

47. Jenkins MW, Chughtai OQ, Basavanhally AN, Watanabe M, Rollins AM (2007) In vivo gated 4D imaging of the embryonic heart using gated optical coherence tomography.  Journal of Biomedical Optics 12, 030505. PMID: 17614708.

48. Qu X, Lam  E, Doughman YQ, Chen  Y, Chou Y-T, Lam M, Turakhia M, Dunwoodie SL, Watanabe M, Xu B, Duncan SA, Yang Y-C (2007) Cited2, a coactivator of HNF4a is essential for liver development. EMBO J 26(21), 4445-4456. PMID: 17932483,  PMCID: PMC2063472.

49. Montano MM, Doughman Y-Q, Deng H, Chapman L, Yang J, Wang N, Zhou Q, Ward NL, Watanabe M. (2008) Mutation of the HEXIM1 gene results in defects during heart and vascular development partly through down regulation of VEGF. Circulation Research. 102(4), 415-422. PMID: 18079413. NIHMSID 219171

50. Xu, B, Qu X, Gu S, Doughman Y-Q, Watanabe M, Yang Y-C.  (2008) Cited2 is required for fetal lung maturation.  Developmental Biology 317(1), 95-105. PMID: 18358466, PMCID: PMC2467387.


51. Chen Y, Doughman Y-Q, Gu S, Jarrell A, Aota S, Cveki A, Watanabe M, Dunwoodie S, Johnson RS,van Heyningen V, Kleinjan D, Beebe D, Yang Y-C. (2008)  Cited2 is required for the proper formation of the hyaloid vasculature and lens morphogenesis. Development 135 (17), 2939-2948, PMCID: PMC2654719.

52. Newbern J, Zhong J, Wickramasinghe SR, Li X, Wu Y, Samuels I, Cherosky N, Karlo JC, O’Loughlin B, Wikenheiser J, Gargesha M, Doughman YQ, Charron J, Ginty DD, Watanabe M, Saitta S, Snider WD, Landreth GE (2008) Mouse and human phenotypes indicate a critical conserved role for the ERK2 signaling pathway in neural crest development. PNAS USA. 105(44) 17115-20. PMID 18952847.  PMCID PMC2579387.

53. Yang K, Doughman YQ, Karunamuni G, Gu S, Yang Y-C, Watanabe M. (2009) Expression of active Notch1 in avian coronary development. Dev Dyn 238(1), 162-170. PMID 19097050. PMID:PMC2929638.

54. Wikenheiser J, Wolfram J, Gargesha M, Yang K, Karunamuni G, Wilson DL, Semenza GL, Agani F, Fisher SA, Ward N, Watanabe M. (2009) Altered hypoxia-inducible factor-1 alpha expression levels correlate with coronary vessel anomalies.  Dev Dyn 238(10), 2688-2700. PMID 1977592. PMC3724469.

55. Karunamuni, G, Yang K, Doughman YQ, Wikenheiser J, Bader  D, Barnett J, Austin A, Parsons-Wingerter P, and Watanabe M. (2010) Expression of lymphatic markers during avian and mouse cardiogenesis. Anatomical Record 293(2), 259-270. PMID 19938109. NIHMSID PMID: PMC287022

56. Jenkins MW, Duke AR, Chiel HJ, Watanabe M, Jansen ED, Rollins AM (2010) Optical pacing of the embryonic heart.  Nature Photonics 4, 623-626. PMCID: PMC3059323

57. Ogba N, Doughman YQ, Chaplin LJ, Hu Y, Gargesha M, Watanabe M, Montano M (2010) HEXIM1 modulates vascular endothelial growth factor expression and function in breast cancer cells and mammary gland. Oncogene 24(25), 3639-49. PMID: 20453883. PMCID:PMC2892028.

58. Haldar SM, Lu Y, Jeyaraj D, Kawanami D, Cui Y, Eapen SJ, Hao C, Li Y, Doughman YQ, Watanabe M, Shimizu K, Kuivaniemi H, Sadoshima J, Margulies KB, Cappola TP, and Jain MK (2010) Klf15 deficiency is a molecular link between heart failure and aortic aneurysm formation. Science Translational Medicine Apr 7;2(26):26ra26. PMID: 20375365. PMCID:PMC3003709.

59. Jenkins MW, Peterson L, Gu S, Gargesha M, Wilson DL, Watanabe M, Rollins AM (2010) Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography.  J Biomed Opt 15(6):066022. PMID:21189196. PMCID: PMC3017576.

60. Gargesha M, Mohammed QQ, Roy D, Steyer GJ, Watanabe M, Wilson DL (2011)
Visualization of color anatomy and molecular fluorescence in whole-mouse cryo-imaging. Comput Med Imaging Graph 35(3):195-205. PMCID: PMC3049862 (Available on 2012/4/1)

61. Garita B, Jenkins M, Han M, Zhou C, VanAuker M, Rollins A, Watanabe M, Fujimoto J, and Linask K. (2011) Blood flow dynamics of one cardiac cycle and relationship to mechanotransduction and trabeculation during heart looping. Am J Physiol Heart Circ Physiol 300(3):H879-891. PMCID:PMC3064308

62. Gu S, Jenkins M, Peterson L, Doughman YQ, Rollins A, Watanabe M (2012). Optical coherence tomography captures rapid hemodynamic responses to acute hypoxia of the cardiovascular system of early embryos. Dev Dyn. 241(3), 534-544. PMID 22275053. PMCID:PMC 3295592

63. Huang TQ, Wang Y, Ebrahem Q, Chen Y, Cheng C, Doughman YQ, Watanabe M, Dunwoodie SL, Yang YC (2012) Deletion of HIF-1α partially rescues the abnormal hyaloid vascular system in Cited2 conditional knockout mouse eyes. Mol Vis. 2012;18:1260-70. Epub 2012 May 11. PMID: 22665973. PMC3365139

64. Peterson LM, Jenkins MW, Gu S, Barwick L, Doughman YQ, Watanabe M, Rollins AM (2012)  4-D Shear Stress Maps of the Developing Heart using Doppler Optical Coherence Tomography. Biomedical Optics Express 3(11), 3022-3032. (Featured in special commentary.) PMC3493225.

65. Krishnamurthy N, Hu Y, Siedlak S, Doughman YQ, Watanabe M, Montano MM.Induction of quinine reductase by tamoxifen or DPN protects against mammary tumorigenesis.  FASEB J. 2012 25(10) 3993-4002. PMC3687752.

66.  Wikenheiser J, Karunamuni G, Sloter E, Walker MK, Roy D, Wilson DL, Watanabe M (2013) Altering HIF-1a through 2,3,7,8-Tetrachlorodibenzo-p-Dioxin (TCDD) exposure affects coronary vessel development. Cardiovascular Toxicology 13(2), 161-7. PMC3632717.

67. Tao J, Doughman YQ, Yang K, Ramirez-Bergeron D, Watanabe M (2013) Epicardial HIF signaling regulates vascular precursor cell invasion into the myocardium Development Biology 376(2),136-49. PMC444961

68. Montano M, Desjardins C, Hsieh Y-H, Hu Y, Wang C, Stelzer J, Dick T, Hoit B, Chandler MP,  Yu X, Watanabe M (2013) Inducible reexpression of HEXIM1 activates a physiological rather than a pathological response in the adult heart. Cardiovascular Research 99(1), 74-82. PMC3687752.

69. Jenkins, MW; Wang YT, Doughman YQ, Watanabe M; Cheng Y; Rollins AM (2013) Optical pacing of the adult rabbit heart. Biomedical Optics Express 4(9), 1626-1635.  PMC in process

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