Hypoxic conditions alter developing branchial arch-derived structures in zebrafish

Trish E Parsons, Seth M Weinberg, Michael Tsang, Alexandre R Vieira

Abstract


Background: Previous epidemiological findings have implicated hypoxia as a risk factor for craniofacial defects including cleft lip, microtia and branchial arch anomalies. This study tests the hypothesis that hypoxic exposure results in craniofacial shape variation in a zebrafish model.

Methods: Three sets of zebrafish embryos were raised in uniform conditions with the exception of dissolved oxygen level.  At 24 hours past fertilization (hpf) embryos were placed in hypoxic conditions (70% or 50% dissolved oxygen tank water) and compared to unexposed control embryos.  After 24 hours of exposure to hypoxia, the embryos were incubated under normoxia.  Larvae were collected at 5 days post fertilization (dpf) and stained for cartilage. Images were taken of each specimen and subsequently landmarked to capture viscerocranial morphology.  A geometric morphometric analysis was performed to compare shape variation across groups.

Results: The mean branchial arch shape of each exposure group was significantly different from controls (p<0.001).  Principal components analysis revealed a clear separation of the three groups, with controls at one end of the shape spectrum, the 50% hypoxia group at the other end, and the 70% hypoxia group spanning the variation in between.

Conclusions: This experiment shows that hypoxia exposure at 24hpf is capable of affecting craniofacial shape in a dose-dependent manner.  These results may have implications not only for high altitude fetal health, but other environments, behaviors and genes that affect fetal oxygen delivery.

 


Full Text:

PDF

References


Unraveling human cleft lip and palate research. Vieira AR. J Dent Res. 2008 Feb;87(2):119-25. Review. PMID: 18218836.

Altitude as a risk factor for congenital anomalies. Castilla EE, Lopez-Camelo JS, Campaña H. Am J Med Genet. 1999 Sep 3;86(1):9-14. PMID: 10440822.

Hyperoxia and hypoxia in pregnancy: simple experimental manipulation alters the incidence of cleft lip and palate in CL/Fr mice. Millicovsky G, Johnston MC. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5722-3. PMID: 6946511.

The effect of hypoxia on facial shape variation and disease phenotypes in chicken embryos. Smith F, Hu D, Young NM, Lainoff AJ, Jamniczky HA, Maltepe E, Hallgrimsson B, Marcucio RS. Dis Model Mech. 2013 Jul;6(4):915-24. doi: 10.1242/dmm.011064. Epub 2013 Apr 16. PMID: 23592613.

Prevalence rates of microtia in South America. Castilla EE, Orioli IM. Int J Epidemiol. 1986 Sep;15(3):364-8. PMID: 3771073.

Nüsslein-Volhard C, Gilmour DT, Dahm R (2002) Zebrafish as a system to study development and organogenesis. In: Nüsslein-Volhard C, Dahm R, editors. Zebrafish; A practical approach. New York: Oxford University Press. pp. 1-5.

Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Kajimura S, Aida K, Duan C. Proc Natl Acad Sci U S A. 2005 Jan 25;102(4):1240-5. Epub 2005 Jan 11. PMID: 15644436.

Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxia-inducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1 gene expression. Kajimura S, Aida K, Duan C. Mol Cell Biol. 2006 Feb;26(3):1142-55. PMID: 16428465.

Molecular dissection of craniofacial development using zebrafish. Yelick PC, Schilling TF. Crit Rev Oral Biol Med. 2002;13(4):308-22. Review. PMID: 12191958.

Sperber GH, Sperber SM, Guttman GD (2010) Craniofacial Embryogenetics and Development. Shelton: People's Medical Publishing House. 251p.

Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Piotrowski T1, Schilling TF, Brand M, Jiang YJ, Heisenberg CP, Beuchle D, Grandel H, van Eeden FJ, Furutani-Seiki M, Granato M, Haffter P, Hammerschmidt M, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Warga RM, Nüsslein-Volhard C. Development. 1996 Dec;123:345-56. PMID: 9007254.

Asymmetric patterns in the cranial skeleton of zebrafish (Danio rerio) exposed to sodium pentachlorophenate at different embryonic developmental stages. López-Romero F1, Zúñiga G, Martínez-Jerónimo F. Ecotoxicol Environ Saf. 2012 Oct;84:25-31. doi: 10.1016/j.ecoenv.2012.06.008. Epub 2012 Jul 19. PMID: 22818112.

Geometric morphometrics: ten years of progress following the ‘Revolution.’ Adams, DC, Rohlf JF, Slice DE. Ital J Zool. 2002 Jan;71:5-16.

Albertson RC, Yelick PC (2009) Morphogenesis of the jaw: Development beyond the embryo. In: Dietrich III HW, Westerfield M, Zon LI, editors. Essential Zebrafish Methods. Boston: Elsevier. pp. 457-477.

Rohlf FJ (1990) Rotational fit (Procrustes) methods. In: Rohlf FJ, Bookstein FL, editors. Proceedings of the Michigan Morphometrics Workshop. Ann Arbor: University of Michigan Museum of Zoolog. pp. 227-236.

Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. San Diego: Elsevier Academic Press. 478 p.

MorphoJ: an integrated software package for geometric morphometrics. Klingenberg CP. Mol Ecol Resour. 2011 Mar;11(2):353-7. doi: 10.1111/j.1755-0998.2010.02924.x. Epub 2010 Oct 5. PMID: 21429143.

Principal warps: Thin-plate splines and the decomposition of deformations. Bookstein FL. IEEE Trans Pattern Anal. 1989 Jun;11(6):567-85.

Schilling TF (2002) The morphology of larval and adult zebrafish. In: Nuessleid-Volhand C, Dalm R, editors. Zebrafish. Oxford: Oxford University Press. pp. 59-94.

Genetic basis of adaptive shape differences in the cichlid head. Albertson RC, Streelman JT, Kocher TD. J Hered. 2003 Jul-Aug;94(4):291-301. PMID: 12920100.

Jaw and branchial arch mutants in zebrafish I: branchial arches. Schilling TF, Piotrowski T, Grandel H, Brand M, Heisenberg CP, Jiang YJ, Beuchle D, Hammerschmidt M, Kane DA, Mullins MC, van Eeden FJ, Kelsh RN, Furutani-Seiki M, Granato M, Haffter P, Odenthal J, Warga RM, Trowe T, Nüsslein-Volhard C. Development. 1996 Dec;123:329-44. PMID: 9007253.

Specification and morphogenesis of the zebrafish larval head skeleton. Kimmel CB, Miller CT, Moens CB. Dev Biol. 2001 May 15;233(2):239-57. Review. PMID: 11336493.

Gorlin R (2001) Branchial arch and co-acral disorders. In: Gorlin R, Hennekam RC, editors. Syndromes of the head and neck. Oxford: Oxford University Press. pp. 790-849.

Examination of a palatogenic gene program in zebrafish. Swartz ME1, Sheehan-Rooney K, Dixon MJ, Eberhart JK. Dev Dyn. 2011 Sep;240(9):2204-20. doi: 10.1002/dvdy.22713. PMID: 22016187.




DOI: https://doi.org/10.5195/d3000.2014.21

Refbacks

  • There are currently no refbacks.