Critical Transitions in Early Embryonic Aortic Arch Patterning and Hemodynamics

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Kowalski, William J ^a   Dur, Onur ^a   Wang, Yajuan ^a   Patrick, Michael J ^b   Tinney, Joseph P ^c   Keller, Bradley B ^a,c   Pekkan, Kerem ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; AORTA ARCH; ARTERIAL WALL THICKNESS; ARTICLE; BLOOD FLOW VELOCITY; CHICK EMBRYO; COMPUTATIONAL FLUID DYNAMICS; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GEOMETRY; HEART HEMODYNAMICS; HEART OUTPUT; HEART SIZE; IMAGE RECONSTRUCTION; MORPHOGENESIS; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; SHEAR STRESS; THREE DIMENSIONAL IMAGING;

ANIMALS; AORTA, THORACIC; CHICK EMBRYO; HEMODYNAMICS;

EID: 84875301461     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060271     Document Type: Article

References (77)

1. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, et al. (2011) Heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation 123: e18-e209.
2. Burggren WW, Keller BB (1998) Development of Cardiovascular Systems: Molecules to Organisms. New York: Cambridge University Press.
3. Pexieder T, (1986) Standardized Method for Study of Normal and Abnormal Cardiac Development in Chick, Rat, Mouse, Dog and Human Embryos. Teratology 33: 91C-92C.
4. Patten BM (1920) The early embryology of the chick. Philadelphia: P. Blakiston's Son & Co. ix, 167 p.
5. Hamburger V, Hamilton HL, (1951) A Series of Normal Stages in the Development of the Chick Embryo. Journal of Morphology 88: 49-92.
6. Manner J, (2000) Cardiac looping in the chick embryo: a morphological review with special reference to terminological and biomechanical aspects of the looping process. Anat Rec 259: 248-262.
7. Martinsen BJ, (2005) Reference guide to the stages of chick heart embryology. Dev Dyn 233: 1217-1237.
8. Hiruma T, Hirakow R, (1995) Formation of the pharyngeal arch arteries in the chick embryo. Observations of corrosion casts by scanning electron microscopy. Anat Embryol (Berl) 191: 415-423.
9. Kardong KV (2009) Vertebrates: comparative anatomy, function, evolution. Boston: McGraw-Hill Higher Education.
10. Hughes AFW, (1934) On the development of the blood vessels in the head of the chick. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 224: 75-U42.
11. Kastschenko N (1887) Das schlundspaltengebiet des Huhnchens. Arch f anat u Physiol, Anat Abt: 258-300.
12. Pexieder T, (1969) Some quantitative aspects on the development of aortic arches in chick embryos between the 2nd and 8th day of incubation. Folia Morphol (Praha) 17: 102-136.
13. Sabin FR, (1917) Development of the primitive vessels of the chick and of the pig. Contributions to Embryology 6: 63-U16.
14. Henning AL, Jiang MX, Yalcin HC, Butcher JT, (2011) Quantitative three-dimensional imaging of live avian embryonic morphogenesis via micro-computed tomography. Dev Dyn 240: 1949-1957.
15. Smith BR, Effmann EL, Johnson GA, (1992) MR microscopy of chick embryo vasculature. J Magn Reson Imaging 2: 237-240.
16. Yelbuz TM, Choma MA, Thrane L, Kirby ML, Izatt JA, (2002) Optical coherence tomography: a new high-resolution imaging technology to study cardiac development in chick embryos. Circulation 106: 2771-2774.
17. Stewart DE, Kirby ML, Sulik KK, (1986) Hemodynamic changes in chick embryos precede heart defects after cardiac neural crest ablation. Circulation Research 59: 545-550.
18. Bayer IM, Adamson SL, Langille BL, (1999) Atrophic remodeling of the artery-cuffed artery. Arterioscler Thromb Vasc Biol 19: 1499-1505.
19. Kamiya A, Bukhari R, Togawa T, (1984) Adaptive regulation of wall shear stress optimizing vascular tree function. Bull Math Biol 46: 127-137.
20. Kamiya A, Togawa T, (1980) Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol 239: H14-21.
21. Lu X, Zhao JB, Wang GR, Gregersen H, Kassab GS, (2001) Remodeling of the zero-stress state of femoral arteries in response to flow overload. Am J Physiol Heart Circ Physiol 280: H1547-1559.
22. Culver JC, Dickinson ME, (2010) The effects of hemodynamic force on embryonic development. Microcirculation 17: 164-178.
23. Rodbard S, (1975) Vascular caliber. Cardiology 60: 4-49.
24. Girerd X, London G, Boutouyrie P, Mourad JJ, Safar M, et al. (1996) Remodeling of the radial artery in response to a chronic increase in shear stress. Hypertension 27: 799-803.
25. Langille BL, O'Donnell F, (1986) Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 231: 405-407.
26. Chen CY, Patrick MJ, Corti P, Kowalski WJ, Roman BL, et al. (2012) Early embryonic great-vessel microcirculation in zebrafish using high-speed confocal μPIV and volume-of-fluid methods. Biorheology 48: 1-17.
27. Corti P, Young S, Chen CY, Patrick MJ, Rochon ER, et al. (2011) Interaction between alk1 and blood flow in the development of arteriovenous malformations. Development 138: 1573-1582.
28. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, et al. (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421: 172-177.
29. Sedmera D, Pexieder T, Rychterova V, Hu N, Clark EB, (1999) Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254: 238-252.
30. Reckova M, Rosengarten C, deAlmeida A, Stanley CP, Wessels A, et al. (2003) Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circulation Research 93: 77-85.
31. Lucitti JL, Tobita K, Keller BB, (2005) Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo. Journal of Experimental Biology 208: 1877-1885.
32. Tobita K, Garrison JB, Liu LJ, Tinney JP, Keller BB, (2005) Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. The anatomical record Part A, Discoveries in molecular, cellular, and evolutionary biology 283: 193-201.
33. deAlmeida A, McQuinn T, Sedmera D, (2007) Increased ventricular preload is compensated by myocyte proliferation in normal and hypoplastic fetal chick left ventricle. Circulation Research 100: 1363-1370.
34. Gessner IH, (1966) Spectrum of congenital cardiac anomalies produced in chick embryos by mechanical interference with cardiogenesis. Circulation Research 18: 625-633.
35. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE, (1999) Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc Res 41: 87-99.
36. Hu N, Christensen DA, Agrawal AK, Beaumont C, Clark EB, et al. (2009) Dependence of aortic arch morphogenesis on intracardiac blood flow in the left atrial ligated chick embryo. Anatomical record 292: 652-660.
37. Rychter Z, (1962) Experimental morphology of the aortic arches and the heart loop in chick embryos. Advances in Morphogenesis 2: 333-371.
38. Rychter Z, Lemez L (1965) Changes in localization in aortic arches of laminar blood streams of main venous trunks to heart after exclusion of vitelline vessels on second day of incubation. Fed Proc Transl Suppl 24: 815-820.
39. Wang Y, Dur O, Patrick MJ, Tinney JP, Tobita K, et al. (2009) Aortic arch morphogenesis and flow modeling in the chick embryo. Annals of Biomedical Engineering 37: 1069-1081.
40. McElhinney DB, Tworetzky W, Lock JE, (2010) Current status of fetal cardiac intervention. Circulation 121: 1256-1263.
41. Mujumdar RB, Ernst LA, Mujumdar SR, Lewis CJ, Waggoner AS, (1993) Cyanine dye labeling reagents: sulfoindocyanine succinimidyl esters. Bioconjug Chem 4: 105-111.
42. Bland JM, Altman DG, (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1: 307-310.
43. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, et al. (1991) Optical coherence tomography. Science 254: 1178-1181.
44. Chen C-Y, Menon PG, Kowalski W, Pekkan K, (2012) Time-resolved OCT-μPIV: a new microscopic PIV technique for noninvasive depth-resolved pulsatile flow profile acquisition. Experiments in Fluids 54: 1-9.
45. Berlien Müller (1997) Angewandte Lasermedizin: Ecomed.
46. Boulnois J-L, (1986) Photophysical processes in recent medical laser developments: A review. Lasers in Medical Science 1: 47-66.
47. Parrish JA, (1981) New concepts in therapeutic photomedicine: photochemistry, optical targeting and the therapeutic window. J Invest Dermatol 77: 45-50.
48. Fercher AF, Drexler W, Hitzenberger CK, Lasser T, (2003) Optical coherence tomography - principles and applications. Reports on Progress in Physics 66: 239-303.
49. Dur O, Coskun TS, Coskun OK, Frakes D, Kara LB, et al. (2011) Computer-Aided Patient-Specific Coronary Artery Graft Design Improvements Using CFD Coupled Shape Optimizer Cardiovascular Engineering and Technology. 2: 35-47.
50. Al-Roubaie S, Jahnsen ED, Mohammed M, Henderson-Toth C, Jones EA, (2011) Rheology of embryonic avian blood. Am J Physiol Heart Circ Physiol 301: H2473-2481.
51. Yoshigi M, Knott GD, Keller BB, (2000) Lumped parameter estimation for the embryonic chick vascular system: a time-domain approach using MLAB. Comput Methods Programs Biomed 63: 29-41.
52. Hu N, Clark EB, (1989) Hemodynamics of the stage 12 to stage 29 chick embryo. Circulation Research 65: 1665-1670.
53. Beloussov LV, (2008) Mechanically based generative laws of morphogenesis. Phys Biol 5: 015009.
54. Taber LA, (2009) Towards a unified theory for morphomechanics. Philos Transact A Math Phys Eng Sci 367: 3555-3583.
55. Taber LA, Eggers DW, (1996) Theoretical study of stress-modulated growth in the aorta. J Theor Biol 180: 343-357.
56. Taber LA, Ng S, Quesnel AM, Whatman J, Carmen CJ, (2001) Investigating Murray's law in the chick embryo. J Biomech 34: 121-124.
57. Broekhuizen ML, Hogers B, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC, et al. (1999) Altered hemodynamics in chick embryos after extraembryonic venous obstruction. Ultrasound in obstetrics & gynecology: the official journal of the International Society of Ultrasound in Obstetrics and Gynecology 13: 437-445.
58. Broekhuizen ML, Mast F, Struijk PC, van der Bie W, Mulder PG, et al. (1993) Hemodynamic parameters of stage 20 to stage 35 chick embryo. Pediatr Res 34: 44-46.
59. Clark EB, Hu N, (1982) Developmental hemodynamic changes in the chick embryo from stage 18 to 27. Circulation Research 51: 810-815.
60. Lucitti JL, Visconti R, Novak J, Keller BB, (2006) Increased arterial load alters aortic structural and functional properties during embryogenesis. Am J Physiol Heart Circ Physiol 291: H1919-1926.
61. Ursem NT, Struijk PC, Poelmann RE, Gittenberger-de Groot AC, Wladimiroff JW, (2001) Dorsal aortic flow velocity in chick embryos of stage 16 to 28. Ultrasound in medicine & biology 27: 919-924.
62. Kowalski WJ, Teslovich NC, Dur O, Keller BB, Pekkan K, (2012) Computational hemodynamic optimization predicts dominant aortic arch selection is driven by embryonic outflow tract orientation in the chick embryo. Biomech Model Mechanobiol 11: 1057-1073.
63. Hacking WJ, VanBavel E, Spaan JA, (1996) Shear stress is not sufficient to control growth of vascular networks: a model study. Am J Physiol 270: H364-375.
64. Hudetz AG, Kiani MF, (1992) The role of wall shear stress in microvascular network adaptation. Adv Exp Med Biol 316: 31-39.
65. Keenan RL, Rodbard S, (1973) Competition between collateral vessels. Cardiovasc Res 7: 670-675.
66. Yashiro K, Shiratori H, Hamada H, (2007) Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 450: 285-288.
67. Milnor WR (1989) Hemodynamics. Baltimore: Williams & Wilkins. xii, 419 p.
68. Watanabe M, Choudhry A, Berlan M, Singal A, Siwik E, et al. (1998) Developmental remodeling and shortening of the cardiac outflow tract involves myocyte programmed cell death. Development 125: 3809-3820.
69. Groenendijk BC, Hierck BP, Gittenberger-De Groot AC, Poelmann RE, (2004) Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Dev Dyn 230: 57-68.
70. Egorova AD, Van der Heiden K, Van de Pas S, Vennemann P, Poelma C, et al. (2011) Tgfbeta/Alk5 signaling is required for shear stress induced klf2 expression in embryonic endothelial cells. Dev Dyn 240: 1670-1680.
71. Wang J, Nagy A, Larsson J, Dudas M, Sucov HM, et al. (2006) Defective ALK5 signaling in the neural crest leads to increased postmigratory neural crest cell apoptosis and severe outflow tract defects. BMC Dev Biol 6: 51.
72. Molin DG, Poelmann RE, DeRuiter MC, Azhar M, Doetschman T, et al. (2004) Transforming growth factor beta-SMAD2 signaling regulates aortic arch innervation and development. Circ Res 95: 1109-1117.
73. Waldo KL, Hutson MR, Ward CC, Zdanowicz M, Stadt HA, et al. (2005) Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Developmental Biology 281: 78-90.
74. Groenendijk BCW, Hierck BP, Gittenberger-de Groot AC, Poelmann RE, (2003) Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Developmental Dynamics 230: 57-68.
75. Poelmann RE, Gittenberger-de Groot AC, Hierck BP, (2008) The development of the heart and microcirculation: role of shear stress. Med Biol Eng Comput 46: 479-484.
76. Anderson MJ, Pham VN, Vogel AM, Weinstein BM, Roman BL, (2008) Loss of unc45a precipitates arteriovenous shunting in the aortic arches. Dev Biol 318: 258-267.
77. DeRuiter MC, Poelmann RE, Mentink MM, Vaniperen L, Gittenberger-De Groot AC, (1993) Early formation of the vascular system in quail embryos. Anat Rec 235: 261-274.