Biophysical mechanisms of cardiac looping.

During early embryogenesis, the heart is a single, relatively straight tube which bends and twists (loops) rightward to create the basic plan of the mature heart. Despite intensive study for many decades, the biophysical mechanisms which drive and regulate cardiac looping have remained poorly understood. This review discusses, from a historical perspective, studies of looping mechanics and various theories which have been proposed for this complex process. Then, based on recently acquired data, a new biomechanical hypothesis is proposed for the rst phase of looping (c-looping). Understanding morphogenetic mechanisms would facilitate research devoted to preventing and treating congenital heart malformations caused by looping abnormalities.

[1]  D. Moskophidis,et al.  Targeted inactivation of the sodium‐calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[2]  R. Rosenberg,et al.  Role of heparan sulfate in dextral heart looping in chick. , 2004, Glycobiology.

[3]  R. Waterman,et al.  Myocardial cell shape change as a mechanism of embryonic heart looping. , 1972, Developmental biology.

[4]  F. Manasek,et al.  Cytodifferentiation: a causal antecedent of looping? , 1978, Birth defects original article series.

[5]  M. E. Flynn,et al.  The mechanism of cervical flexure formation in the chick , 2004, Anatomy and Embryology.

[6]  F. Manasek,et al.  Experimental studies of the shape and structure of isolated cardiac jelly. , 1978, Journal of embryology and experimental morphology.

[7]  E. Brouzes,et al.  Interplay of mechanical deformation and patterned gene expression in developing embryos. , 2004, Current opinion in genetics & development.

[8]  M. Kirby,et al.  Wherefore heart thou? Embryonic origins of cardiogenic mesoderm , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[9]  Gabriel Acevedo-Bolton,et al.  Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis , 2003, Nature.

[10]  L. V. Belousov,et al.  The Dynamic Architecture of a Developing Organism: An Interdisciplinary Approach to the Development of Organisms , 1998 .

[11]  M. Yasuda,et al.  Changes in the arrangement of actin bundles during heart looping in the chick embryo , 2004, Anatomy and Embryology.

[12]  Larry A Taber,et al.  On the effects of residual stress in microindentation tests of soft tissue structures. , 2004, Journal of biomechanical engineering.

[13]  M. Brueckner,et al.  Cilia propel the embryo in the right direction. , 2001, American journal of medical genetics.

[14]  N. J. Sissman,et al.  Cell Multiplication Rates During Development of the Primitive Cardiac Tube in the Chick Embryo , 1966, Nature.

[15]  Larry A Taber,et al.  The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo. , 2004, Developmental biology.

[16]  R. Harvey,et al.  Cardiac looping--an uneasy deal with laterality. , 1998, Seminars in cell & developmental biology.

[17]  F. Manasek.  Control of early embryonic heart morphogenesis: a hypothesis. , 1983, Ciba Foundation symposium.

[18]  T. Schlange,et al.  Effects of antisense misexpression of CFC on downstream flectin protein expression during heart looping , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[19]  Correlation of gene expression with physiological functions: Examples of pulmonary blood vessel rheology, hypoxic hypertension, and tissue remodeling. , 2001, Biorheology.

[20]  K. Linask,et al.  A role for fibronectin in the migration of avian precardiac cells. II. Rotation of the heart-forming region during different stages and its effects. , 1988, Developmental biology.

[21]  K. Linask,et al.  Precardiac cell migration: fibronectin localization at mesoderm-endoderm interface during directional movement. , 1986, Developmental biology.

[22]  B. M. Patten.  Early embryology of the chick , 2009 .

[23]  J. Nora,et al.  Congenital heart disease : causes and processes , 1984 .

[24]  L A Taber,et al.  Mechanics of cardiac looping , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[25]  Elliot L Elson,et al.  Role of actin polymerization in bending of the early heart tube , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[26]  K. Linask.  Regulation of heart morphology: current molecular and cellular perspectives on the coordinated emergence of cardiac form and function. , 2003, Birth defects research. Part C, Embryo today : reviews.

[27]  K. Shiokawa,et al.  The behavior and cytoskeletal system of chick gastrula mesodermal cells on substrata coated with lines of fibronectin. , 1991, The Journal of experimental zoology.

[28]  Le A. Trinh,et al.  Fibronectin regulates epithelial organization during myocardial migration in zebrafish. , 2004, Developmental cell.

[29]  Larry A Taber,et al.  Material properties and residual stress in the stage 12 chick heart during cardiac looping. , 2004, Journal of biomechanical engineering.

[30]  T. Delhaas,et al.  Cardiac Fiber Orientation and the Left‐Right Asymmetry Determining Mechanism , 2004, Annals of the New York Academy of Sciences.

[31]  A. Romanoff.  The avian embryo. Structural and functional development. , 1960 .

[32]  K. Linask,et al.  Directionality of heart looping: effects of Pitx2c misexpression on flectin asymmetry and midline structures. , 2002, Developmental biology.

[33]  H. Stalsberg,et al.  The precardiac areas and formation of the tubular heart in the chick embryo. , 1969, Developmental biology.

[34]  H. Stalsberg,et al.  Development and ultrastructure of the embryonic heart. II. Mechanism of dextral looping of the embryonic heart. , 1970, The American journal of cardiology.

[35]  D. Srivastava,et al.  Knowing in your heart what's right. , 1997, Trends in cell biology.

[36]  Gabriel Fenteany,et al.  Small-molecule inhibitors of actin dynamics and cell motility. , 2003, Current topics in medicinal chemistry.

[37]  G. Steding,et al.  Correlation between the embryonic head flexures and cardiac development , 1993, Anatomy and Embryology.

[38]  K. Linask,et al.  A role for fibronectin in the migration of avian precardiac cells. I. Dose-dependent effects of fibronectin antibody. , 1988, Developmental biology.

[39]  J. McLachlan,et al.  Looping of chick embryo hearts in vitro. , 1990, Journal of anatomy.

[40]  Jörg Männer,et al.  On rotation, torsion, lateralization, and handedness of the embryonic heart loop: new insights from a simulation model for the heart loop of chick embryos. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[41]  Thomas Brand,et al.  Heart development: molecular insights into cardiac specification and early morphogenesis. , 2003, Developmental biology.

[42]  H. Baldwin,et al.  Degradation of hyaluronic acid does not prevent looping of the mammalian heart in situ. , 1989, Developmental biology.

[43]  I. Shiraishi,et al.  3-D observation of actin filaments during cardiac myofibrinogenesis in chick embryo using a confocal laser scanning microscope , 1992, Anatomy and Embryology.

[44]  Jörg Männer,et al.  Cardiac looping in the chick embryo: A morphological review with special reference to terminological and biomechanical aspects of the looping process , 2000, The Anatomical record.

[45]  J. A. Los,et al.  Isomyosin expression pattern during formation of the tubular chicken heart: A three‐dimensional immunohistochemical analysis , 1990, The Anatomical record.

[46]  R. Bellairs.  Studies on the Development of the Foregut in the Chick Blastoderm 1. The Presumptive Foregut Area , 1953 .

[47]  H. Stalsberg.  The origin of heart asymmetry: right and left contributions to the early chick embryo heart. , 1969, Developmental biology.

[48]  N. Hirokawa,et al.  Randomization of Left–Right Asymmetry due to Loss of Nodal Cilia Generating Leftward Flow of Extraembryonic Fluid in Mice Lacking KIF3B Motor Protein , 1999, Cell.

[49]  M Levin,et al.  Left-right asymmetry determination in vertebrates. , 2001, Annual review of cell and developmental biology.

[50]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[51]  Left-right asymmetry: Nodal points , 2003, Journal of Cell Science.

[52]  R. Zak,et al.  Growth of the heart in health and disease , 1984 .

[53]  M. Bronner‐Fraser,et al.  N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. , 2000, Science.

[54]  J. Icardo,et al.  Effects of colchicine on the formation and looping of the tubular heart of the embryonic chick. , 1984, Acta anatomica.

[55]  O. Piro,et al.  Fluid-dynamical basis of the embryonic development of left-right asymmetry in vertebrates. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[56]  N. Hirokawa,et al.  Abnormal nodal flow precedes situs inversus in iv and inv mice. , 1999, Molecular cell.

[57]  L. Taber,et al.  Mechanical Asymmetry in the Embryonic Chick Heart During Looping , 2003, Annals of Biomedical Engineering.

[58]  Larry A Taber,et al.  Cardiac looping in experimental conditions: Effects of extraembryonic forces , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[59]  B. M. Patten,et al.  The formation of the cardiac loop in the chick , 1922 .

[60]  S. Chacko,et al.  The effect of 5-bromodeoxyuridine (BrdU) on cardiac muscle differentiation. , 1974, Developmental biology.

[61]  Wei Huang,et al.  Tissue Remodeling of Rat Pulmonary Artery in Hypoxic Breathing. I. Changes of Morphology, Zero-Stress State, and Gene Expression , 2004, Annals of Biomedical Engineering.

[62]  H. Stalsberg,et al.  Regional mitotic activity in the precardiac mesoderm and differentiating heart tube in the chick embryo. , 1969, Developmental biology.

[63]  Manasek Fj,et al.  The birth defects conferences: the last ten years and the next. , 1978 .

[64]  K. Linask,et al.  Differential expression of flectin in the extracellular matrix and left-right asymmetry in mouse embryonic heart during looping stages. , 1998, Developmental genetics.

[65]  R. Schwartz,et al.  Rho kinases play an obligatory role in vertebrate embryonic organogenesis. , 2001, Development.

[66]  D. Supp,et al.  Molecular motors: the driving force behind mammalian left-right development. , 2000, Trends in cell biology.

[67]  R. Hirakow,et al.  An ultrastructual topographical study on myofibrillogenesis in the heart of the chick embryo during pulsation onset period , 2004, Anatomy and Embryology.

[68]  J. Howard,et al.  Mechanics of Motor Proteins and the Cytoskeleton , 2001 .

[69]  Mineo Yasuda,et al.  Actin bundles on the right side in the caudal part of the heart tube play a role in dextro-looping in the embryonic chick heart , 2004, Anatomy and Embryology.

[70]  Y. Saijoh,et al.  Determination of left–right patterning of the mouse embryo by artificial nodal flow , 2002, Nature.

[71]  N. Philp,et al.  Left-right asymmetric localization of flectin in the extracellular matrix during heart looping. , 1996, Developmental biology.

[72]  F J Manasek,et al.  Early cardiac morphogenesis is independent of function. , 1972, Developmental biology.

[73]  R. Dehaan,et al.  Development of Form in the Embryonic Heart An Experimental Approach , 1967, Circulation.