Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Molecular Medicine Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1791-2997 Online ISSN: 1791-3004
Journal Cover
September-2016 Volume 14 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
September-2016 Volume 14 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article Open Access

Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish

  • Authors:
    • Rebecca Powell
    • Ekaterina Bubenshchikova
    • Yayoi Fukuyo
    • Chaonan Hsu
    • Olga Lakiza
    • Hiroki Nomura
    • Erin Renfrew
    • Deborah Garrity
    • Tomoko Obara
  • View Affiliations / Copyright

    Affiliations: Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma, OK 73104, USA, Department of Biology, Colorado State University, Fort Collins, CO 80523, USA
    Copyright: © Powell et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 2665-2678
    |
    Published online on: July 27, 2016
       https://doi.org/10.3892/mmr.2016.5550
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Wilm's tumor 1 interacting protein (Wtip) was identified as an interacting partner of Wilm's tumor protein (WT1) in a yeast two-hybrid screen. WT1 is expressed in the proepicardial organ (PE) of the heart, and mouse and zebrafish wt1 knockout models appear to lack the PE. Wtip's role in the heart remains unexplored. In the present study, we demonstrate that wtip expression is identical in wt1a‑, tcf21‑, and tbx18‑positive PE cells, and that Wtip protein localizes to the basal body of PE cells. We present the first genetic evidence that Wtip signaling in conjunction with WT1 is essential for PE specification in the zebrafish heart. By overexpressing wtip mRNA, we observed ectopic expression of PE markers in the cardiac and pharyngeal arch regions. Furthermore, wtip knockdown embryos showed perturbed cardiac looping and lacked the atrioventricular (AV) boundary. However, the chamber‑specific markers amhc and vmhc were unaffected. Interestingly, knockdown of wtip disrupts early left‑right (LR) asymmetry. Our studies uncover new roles for Wtip regulating PE cell specification and early LR asymmetry, and suggest that the PE may exert non‑autonomous effects on heart looping and AV morphogenesis. The presence of cilia in the PE, and localization of Wtip in the basal body of ciliated cells, raises the possibility of cilia-mediated PE signaling in the embryonic heart.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Figure 7

View References

1 

DeHaan RL: Morphogenesis of the vertebrate heart. Organogenesis. DeHaan RL and Ursprung H: Holt, Rinehart and Winston; New York: pp. 377–419. 1965

2 

Serbedzija GN, Chen JN and Fishman MC: Regulation in the heart field of zebrafish. Development. 125:1095–1101. 1998.PubMed/NCBI

3 

Bagatto B, Francl J, Liu B and Liu Q: Cadherin2 (N-cadherin) plays an essential role in zebrafish cardiovascular development. BMC Dev Biol. 6:232006. View Article : Google Scholar : PubMed/NCBI

4 

Fishman MC and Chien KR: Fashioning the vertebrate heart: Earliest embryonic decisions. Development. 124:2099–2117. 1997.PubMed/NCBI

5 

Mikawa T and Fishman DA: Retroviral analysis of cardiac morphogenesis: Discontinuous formation of coronary vessels. Proc Natl Acad Sci USA. 89:9504–9508. 1992. View Article : Google Scholar : PubMed/NCBI

6 

Mikawa T and Gourdie RG: Pericardial mesoderm generates a populations of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol. 174:221–232. 1996. View Article : Google Scholar : PubMed/NCBI

7 

Dettman RW, Denetclaw W Jr, Ordahl CP and Bristow J: Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol. 193:169–181. 1998. View Article : Google Scholar : PubMed/NCBI

8 

Pérez-Pomares JM, Macías D, García-Garrido L and Munõz-Chápuli R: Immunolocalization of the vascular endothelial growth factor receptor-2 in the subepicardial mesenchyme of hamster embryos: Identification of the coronary vessel precursors. HIstochem J. 30:627–634. 1998. View Article : Google Scholar : PubMed/NCBI

9 

Vrancken Peeters MP, Gittenberger-de Groot AC, Mentink MM and Poelmann RE: Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat Embryol (Berl). 199:367–378. 1999. View Article : Google Scholar

10 

Gittenberger-de Groot AC, Vrancken Petters MP, Bergweff M, Mentink MM and Poelmann RE: Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Cir Res. 87:969–971. 2000. View Article : Google Scholar

11 

Reese DE, Mikawa T and Bader DM: Development of the coronary vessel system. Circ Res. 91:761–768. 2002. View Article : Google Scholar : PubMed/NCBI

12 

von Gise A and Pu WT: Endocardial and epicardial to mesenchymal transitions in heart development and disease. Circ Res. 110:1628–1645. 2012. View Article : Google Scholar : PubMed/NCBI

13 

Manner J: Experimental study on the formation of the epicardium in chick embryos. Anat Embryol (Berl). 187:281–289. 1993. View Article : Google Scholar

14 

Svensson EC: Deciphering the signals specifying the proepiardium. Cir Res. 106:1789–1790. 2010. View Article : Google Scholar

15 

Bakkers J: Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res. 91:279–288. 2011. View Article : Google Scholar : PubMed/NCBI

16 

Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D and Jaenisch R: WT-1 is reqiored for early kidney development. Cell. 74:679–691. 1993. View Article : Google Scholar : PubMed/NCBI

17 

Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA and Laobow MA: Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development. 121:489–503. 1995.PubMed/NCBI

18 

Yang JT, Raybum H and Hynes RO: Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development. 121:549–560. 1995.PubMed/NCBI

19 

Moore AW, Mclnnes L, Kreidberg J, Hastie ND and Schedl A: YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development. 126:1845–1857. 1999.PubMed/NCBI

20 

Red-Horse K, Ueno H, Weissman IL and Krasnow MA: Coronary arteries from by developmental reprogramming of venous cells. Nature. 464:549–553. 2010. View Article : Google Scholar :

21 

von Gise A, Zhou B, Honor LB, Ma Q, Petryk A and Pu WT: WT1 regulates epicardial epithelial to mesenchymal transition through β-catenin and retinoic acid signaling pathways. Dev Biol. 356:421–431. 2011. View Article : Google Scholar : PubMed/NCBI

22 

Serluca FC: Development of the proepicardial organ in the zebrafish. Dev Biol. 315:18–27. 2008. View Article : Google Scholar : PubMed/NCBI

23 

Liu J and Stainier DY: Tbx5 and Bmp signaling are essential for proepicardium specification in zebrafish. Circ Res. 106:1818–1828. 2010. View Article : Google Scholar : PubMed/NCBI

24 

Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG and Poss KD: A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell. 127:607–619. 2006. View Article : Google Scholar : PubMed/NCBI

25 

Kikuchi K, Gupta V, Wang J, Holdway JE, Wills AA, Fang Y and Poss KD: tcf21+ epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development. 138:2895–2902. 2011. View Article : Google Scholar : PubMed/NCBI

26 

Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G and Poss KD: Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dec Cell. 20:397–404. 2011. View Article : Google Scholar

27 

Kim J, Wu Q, Zhang Y, Wiens KM, Huan Y, Rubin N, Shimada H, Handin RI, Chao MY, Tuan TL, et al: PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc Natl Acad Sci USA. 107:17206–17210. 2010. View Article : Google Scholar : PubMed/NCBI

28 

Wu H, Lee SH, Gao J, Liu X and Iruela-Arispe ML: Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development. 126:3597–3605. 1999.PubMed/NCBI

29 

Chen TH, Chang TC, Kang JO, Choudhary B, Makita T, Tran CM, Burch JB, Eid H and Sucov HM: Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev Biol. 250:198–207. 2002. View Article : Google Scholar : PubMed/NCBI

30 

Sengbusch JK, He W, Pinco KA and Yang JT: Dual functions of [alpha]4[beta]1 integrin in epicardial development: Initial migration and long-term attachment. J Cell Biol. 157:873–882. 2002. View Article : Google Scholar : PubMed/NCBI

31 

Hatcher CJ, Diman NY, Kim MS, Pennisi D, Song Y, Goldstein MM, Mikawa T and Basson CT: A role for Tbx5 in proepicardial cell migration during cardiogenesis. Physiol Genomics. 18:129–140. 2004. View Article : Google Scholar : PubMed/NCBI

32 

Schlueter J and Brand T: A right-sided pathway involving FGF8/Snai1 controls asymmetric development of the proepicardium in the chick embryo. Proc Natl Acad Sci USA. 106:7485–7490. 2009. View Article : Google Scholar : PubMed/NCBI

33 

Schulte I, Schlueter J, Abu-Issa R, Brand T and Männer J: Morphological and molecular left-right asymmetries in the development of the proepicardium: A comparative analysis on mouse and chick embryos. Dev Dyn. 236:684–695. 2007. View Article : Google Scholar : PubMed/NCBI

34 

Chen JN, van Eeden FJ, Warren KS, Chin A, Nüsslein-Volhard C, Haffter P and Fishman MC: Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. Development. 124:4373–4382. 1997.PubMed/NCBI

35 

Shu X, Huang J, Dong Y, Choi J, Langenbacher A and Chen JN: Na,K-ATPase alpha2 and Ncx4a regulate zebrafish left-right patterning. Development. 134:1921–1930. 2007. View Article : Google Scholar : PubMed/NCBI

36 

Fakhro KA, Choi M, Ware SM, Belmont JW, Towbin JA, Lifton RP, Khokha MK and Brueckner M: Rare copy number variations in congenital heart disease patients identify unique genes in left-right patterning. Proc Natl Acad Sc USA. 108:2915–2920. 2011. View Article : Google Scholar

37 

Chin AJ, Saint-Jeannet JP and Lo CW: How insights from cardiovascular developmental biology have impacted the care of infants and children with congenital heart disease. Mech Dev. 129:75–97. 2012. View Article : Google Scholar : PubMed/NCBI

38 

Francis RJ, Christopher A, Devine WA, Ostrowski L and Lo C: Congenital heart disease and the specification of left-right asymmetry. Am J Physiol Heart Circ Physiol. 302:H2102–H2111. 2012. View Article : Google Scholar : PubMed/NCBI

39 

Slough J, Cooney L and Brueckner M: Monocilia in the embryonic mouse heart suggest a direct role for cilia in cardiac morphogenesis. Dev Dyn. 237:2304–2314. 2008. View Article : Google Scholar : PubMed/NCBI

40 

Srichai MB, Konieczkowski M, Padiyar A, Konieczkowski DJ, Mukherjee A, Hayden PS, Kamat S, El-Meanawy MA, Khan S, Mundel P, et al: A WT1 co-regulator controls podocyte phenotype by shuttling between adhesion structures and nucleus. J Biol Chem. 279:14398–14408. 2004. View Article : Google Scholar : PubMed/NCBI

41 

van Wijk NV, Witte F, Feike AC, Schambony A, Birchmeier W, Mundlos S and Stricker S: The LIM domain protein Wtip interacts with the receptor tyrosine kinase Ror2 and inhibits canonical Wnt signaling. Biochem Biophys Res Commun. 390:211–216. 2009. View Article : Google Scholar : PubMed/NCBI

42 

Langer EM, Feng Y, Zhaoyuan H, Rauscher FJ III, Kroll KL and Longmore GD: Ajuba LIM proteins are snail/slug corepressors required for neural crest development in Xenopus. Dev Cell. 14:424–436. 2008. View Article : Google Scholar : PubMed/NCBI

43 

Das Thakur M, Feng Y, Jagannathan R, Seppa MJ, Skeath JB and Longmore GD: Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr Biol. 20:657–662. 2010. View Article : Google Scholar : PubMed/NCBI

44 

Bubenshchikova E, Ichimura K, Fukuyo Y, Powell R, Hsu C, Morrical SO, Sedor JR, Sakai T and Obara T: Wtip and Vangl2 are required for mitotic spindle orientation and cloaca morphogenesis. Biol Open. 1:588–596. 2012. View Article : Google Scholar : PubMed/NCBI

45 

Gana S, Veggiotti P, Sciacca G, Fedeli C, Bersano A, Micieli G, Maghnie M, Ciccone R, Rossi E, Plunkett K, et al: 19q13.11 cryptic deletion: Description of two new cases and indication for a role of WTIP haploinsufficiency in hypospadias. Eur J Hum Genet. 20:852–856. 2012. View Article : Google Scholar : PubMed/NCBI

46 

Westerfield M: The Zebrafish Book A Guide For The Laboratory Use Of Zebrafish Danio (Brachydanio) Rerio. 4th edition. University of Oregon Pressm; Eugene, OR: 2000

47 

Feng J, Jia N, Han LN, Huang FS, Xie YF, Liu J and Tang JS: Microinjection of morphine into thalamic nucleus submedius depresses bee venom-induced inflammatory pain in the rat. J Pharm Pharmacol. 60:1355–1363. 2008. View Article : Google Scholar : PubMed/NCBI

48 

Amack JD and Yost HJ: The T box transcription factor no tail in ciliated controls zebrafish left-right asymmetry. Curr Biol. 14:685–690. 2004. View Article : Google Scholar : PubMed/NCBI

49 

Hauptmann G and Gerster T: Multicolor whole-mount in situ hybridization. Methods Mol Biol. 137:139–148. 2000.PubMed/NCBI

50 

Thisse C and Thisse B: High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc. 3:59–69. 2008. View Article : Google Scholar : PubMed/NCBI

51 

Yelon D, Home SA and Stainier DY: Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev Biol. 214:23–37. 1999. View Article : Google Scholar : PubMed/NCBI

52 

Berdougo E, Coleman H, Lee DH, Stainier DY and Yelon D: Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development. 130:6121–6129. 2003. View Article : Google Scholar : PubMed/NCBI

53 

Long S, Ahmad N and Rebagliati M: The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development. 130:2303–2316. 2003. View Article : Google Scholar : PubMed/NCBI

54 

Ahmad I, Pacheco M and Santos MA: Exzymatic and nonenzymatic antioxidants as an adaptaion to phagocyte-induced damage in Anguilla Anguilla L. following in situ harbor water exposure. Exotoxicol Environ Saf. 57:290–302. 2004. View Article : Google Scholar

55 

Chernyavskaya Y, Ebert AM, Milligan E and Garrity DM: Voltage-gated calcium channel CACNB2 (β2.1) protein is required in the heart for control of cell proliferation and heart tube integrity. Dev Dyn. 241:648–662. 2012. View Article : Google Scholar : PubMed/NCBI

56 

Kim S, Zaghloul NA, Bubenshchikova E, Oh EC, Rankin S, Katsanis N, Obara T and Tsiokas L: Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat Cell Biol. 13:351–360. 2011. View Article : Google Scholar : PubMed/NCBI

57 

Pritchard-Jones K, Fleming S, Davison D, Bickmore W, Porteous D, Gosden C, Bard J, Buckler A, Pelletier J, Housman D, et al: The candidate Wilms' tumour gene is involved in genitourinary development. Nature. 346:194–197. 1990. View Article : Google Scholar : PubMed/NCBI

58 

Armstrong JF, Pritchard-Jones K, Bickmore WA, Hastie ND and Bard JB: The expression of the Wilms' tumour gene, WT1, in the developing mammalian embryo. Mech Dev. 40:85–97. 1993. View Article : Google Scholar : PubMed/NCBI

59 

Drummond IA, Majumdar A, Hentschel H, Elger M, Solnica-Krezel L, Schier AF, Neuhauss SC, Stemple DL, Zwartkruis F, Rangini Z, et al: Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development. 125:4655–4667. 1998.PubMed/NCBI

60 

Carmona R, González-Iriarte M, Pérez-Pomares JM and Muñoz-Chápuli R: Localization of the Wilm's tumour protein WT1 in avian embryos. Cell Tissue Res. 303:173–186. 2001. View Article : Google Scholar : PubMed/NCBI

61 

Ichimura K, Bubenshchikova E, Powell R, Fukuyo Y, Nakamura T, Tran U, Oda S, Tanaka M, Wessely O, Kurihara H, et al: A comparative analysis of glomerulus development in the pronephros of medaka and zebrafish. PLoS One. 7:e452862012. View Article : Google Scholar : PubMed/NCBI

62 

Van der Heiden K, Groenendijk BC, Hierck BP, Hogers B, Koerten HK, Mommaas AM, Gittenberger-de Groot AC and Poelmann RE: Monocilia on chicken embryonic endocardium in low shear stress areas. Dev Dyn. 235:19–28. 2006. View Article : Google Scholar

63 

Perner B, Englert C and Bollig F: The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev Biol. 309:87–96. 2007. View Article : Google Scholar : PubMed/NCBI

64 

Auman HJ, Coleman H, Riley HE, Olale F, Tsai HJ and Yelon D: Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol. 5:e532007. View Article : Google Scholar : PubMed/NCBI

65 

Mably JD, Modhideen MA, Burns CG, Chen JN and Fishman MC: Heart of glass regulates the concentric growth of the heart in zebrafish. Curr Biol. 13:2138–2147. 2003. View Article : Google Scholar : PubMed/NCBI

66 

Baker K, Warren KS, Yellen G and Fishman MC: Defective 'pacemaker' current (Ih) in a zebrafish mutant with a slow heart reate. Proc Natl Acad Sci USA. 94:4554–4559. 1997. View Article : Google Scholar

67 

Jacob E, Drexel M, Schwerte T and Pelster B: Influence of hypoxia and of hypoxemia on the development of cardiac activity in zebrafish larvae. Am J Physiol Regul Integr Comp Physiol. 283:R911–R917. 2002. View Article : Google Scholar : PubMed/NCBI

68 

Vermot J, Forouhar AS, Liebling M, Wu D, Plummer D, Gharib M and Fraser SE: Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol. 7:e10002462009. View Article : Google Scholar : PubMed/NCBI

69 

Nagai Y, Asaoka Y, Namae M, Saito K, Momose H, Mitani H, Furutani-Seiki M, Katada T and Nishina H: The LIM protein Ajuba is required for ciliogenesis and left-right axis determination in medaka. Biochem Biophys Res Commun. 396:887–893. 2010. View Article : Google Scholar : PubMed/NCBI

70 

Witzel HR, Jungblut B, Choe CP, Crump JG, Braun T and Dobreva G: The LIM protein Ajuba restricts the second heart field progenitor pool by regulating Isl1 activity. Dev Cell. 23:58–57. 2012. View Article : Google Scholar : PubMed/NCBI

71 

Essner JJ, Vogan KJ, Wagner MK, Tabin CJ, Yost HJ and Brueckner M: Conserved function for embryonic nodal cilia. Nature. 418:37–38. 2002. View Article : Google Scholar : PubMed/NCBI

72 

Essner JJ, Amack JD, Nyholm MK, Harris EB and Yost HJ: Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development. 132:1247–1260. 2005. View Article : Google Scholar : PubMed/NCBI

73 

Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF and Drummond IA: Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development. 132:1907–1921. 2005. View Article : Google Scholar : PubMed/NCBI

74 

Wessely O and Obara T: Fish and frogs: Models for vertebrate cilia signaling. Front Biosci. 13:1866–1880. 2008. View Article : Google Scholar

75 

Swanhart LM, Cosentino CC, Diep CQ, Davidson AJ, de Caestecker M and Hukriede NA: Zebrafish kidney development: basic science to translational research. Birth Defects Res C Embryo Today. 93:141–156. 2011. View Article : Google Scholar : PubMed/NCBI

76 

Brueckner M: Impact of genetic diagnosis on clinical management of patients with congenital heart disease: Cilia point the way. Circulation. 125:2178–2180. 2012. View Article : Google Scholar : PubMed/NCBI

77 

Svensson LG: Percutaneous aortic valves: Effective in inoperable patients, what price in high-ris patients? J Thorac Cardiovasc Surg. 140(6 Suppl): S10–S13; discussion S86–S91. 2010. View Article : Google Scholar : PubMed/NCBI

78 

Poss KD, Wilson LG and Keating MT: Heart regeneration in zebrafish. Science. 298:2188–2190. 2002. View Article : Google Scholar : PubMed/NCBI

79 

Myklebust R, Engedal H, Saetersdai TS and Ulstein M: Primary 9 + 0 cilia in the embryonic and the adult human heart. Anat Embryol (Berl). 151:127–139. 1977. View Article : Google Scholar

80 

Beis D, Bartman T, Jin SW, Scott IC, D'Amico LA, Ober EA, Verkade H, Frantsve J, Field HA, Wehman A, et al: Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development. 132:4193–4204. 2005. View Article : Google Scholar : PubMed/NCBI

81 

Smith KA, Langendijk AK, Courtney AD, Chen H, Paterson D, Hogan BM, Wicking C and Bakkers J: Transmembrane protein 2 (Tmem2) is required to regionally restrict atrioventricular canal boundary and endocardial cushion development. Development. 138:4193–4198. 2011. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Powell R, Bubenshchikova E, Fukuyo Y, Hsu C, Lakiza O, Nomura H, Renfrew E, Garrity D and Obara T: Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish. Mol Med Rep 14: 2665-2678, 2016.
APA
Powell, R., Bubenshchikova, E., Fukuyo, Y., Hsu, C., Lakiza, O., Nomura, H. ... Obara, T. (2016). Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish. Molecular Medicine Reports, 14, 2665-2678. https://doi.org/10.3892/mmr.2016.5550
MLA
Powell, R., Bubenshchikova, E., Fukuyo, Y., Hsu, C., Lakiza, O., Nomura, H., Renfrew, E., Garrity, D., Obara, T."Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish". Molecular Medicine Reports 14.3 (2016): 2665-2678.
Chicago
Powell, R., Bubenshchikova, E., Fukuyo, Y., Hsu, C., Lakiza, O., Nomura, H., Renfrew, E., Garrity, D., Obara, T."Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish". Molecular Medicine Reports 14, no. 3 (2016): 2665-2678. https://doi.org/10.3892/mmr.2016.5550
Copy and paste a formatted citation
x
Spandidos Publications style
Powell R, Bubenshchikova E, Fukuyo Y, Hsu C, Lakiza O, Nomura H, Renfrew E, Garrity D and Obara T: Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish. Mol Med Rep 14: 2665-2678, 2016.
APA
Powell, R., Bubenshchikova, E., Fukuyo, Y., Hsu, C., Lakiza, O., Nomura, H. ... Obara, T. (2016). Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish. Molecular Medicine Reports, 14, 2665-2678. https://doi.org/10.3892/mmr.2016.5550
MLA
Powell, R., Bubenshchikova, E., Fukuyo, Y., Hsu, C., Lakiza, O., Nomura, H., Renfrew, E., Garrity, D., Obara, T."Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish". Molecular Medicine Reports 14.3 (2016): 2665-2678.
Chicago
Powell, R., Bubenshchikova, E., Fukuyo, Y., Hsu, C., Lakiza, O., Nomura, H., Renfrew, E., Garrity, D., Obara, T."Wtip is required for proepicardial organ specification and cardiac left/right asymmetry in zebrafish". Molecular Medicine Reports 14, no. 3 (2016): 2665-2678. https://doi.org/10.3892/mmr.2016.5550
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team