Diversity and convergence in the mechanisms establishing L/R asymmetry in metazoa

EMBO Reports

Volumn 15, Issue 9, 2014, Pages 926-937

  Coutelis, Jean Baptiste ^a   González Morales, Nicanor ^a   Géminard, Charles ^a   Noselli, Stéphane ^a  

^a CENTRE DE BIOCHIMIE   (France)

Author keywords

directional morphogenesis; evolution, invertebrates; L R asymmetry; symmetry breaking; vertebrates

Indexed keywords

ANIMAL; CAENORHABDITIS ELEGANS; CELL STRUCTURE; CHIRALITY; DEUTEROSTOMIA; DROSOPHILA MELANOGASTER; EVOLUTION; FLOW; INVERTEBRATE; ION CURRENT; LEFT RIGHT ASYMMETRY; LYMNAEA; MORPHOGENESIS; NONHUMAN; REVIEW; SPECIES DIVERSITY; VERTEBRATE; EMBRYO DEVELOPMENT; GENETICS; HUMAN;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; EMBRYONIC DEVELOPMENT; HUMANS; INVERTEBRATES; VERTEBRATES;

EID: 84906850253     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201438972     Document Type: Review

References (118)

1. Boycott AE, Diver C, (1923) On the inheritance of sinistrality in Limnaea peregra. Proc R Soc Lond B, Contain Papers Biol Charact 95: 207-213
2. Gurdon JB, (2005) Sinistral snails and gentlemen scientists. Cell 123: 751-753 (Pubitemid 41721019)
3. Danos MC, Yost HJ, (1995) Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development 121: 1467-1474
4. Fujinaga M, Baden JM, (1991) A new method for explanting early postimplantation rat embryos for culture. Teratology 43: 95-100
5. Hoyle C, Brown NA, Wolpert L, (1992) Development of left/right handedness in the chick heart. Development 115: 1071-1078
6. Hummel KP, Chapman DB, (1959) Visceral inversion and associated anomalies in the mouse. J Hered 50: 9-13
7. Layton WM, Layton MW, Binder M, Kurnit DM, Hanzlik AJ, Van Keuren M, Biddle FG, (1993) Expression of the IV (reversed and/or heterotaxic) phenotype in SWV mice. Teratology 47: 595-602 (Pubitemid 23172501)
8. Schreiner CM, Scott WJ Jr, Supp DM, Potter SS, (1993) Correlation of forelimb malformation asymmetries with visceral organ situs in the transgenic mouse insertional mutation, legless. Dev Biol 158: 560-562 (Pubitemid 23243913)
9. Stalsberg H, (1969) The origin of heart asymmetry: right and left contributions to the early chick embryo heart. Dev Biol 19: 109-127
10. Yokoyama T, Copeland NG, Jenkins NA, Montgomery CA, Elder FF, Overbeek PA, (1993) Reversal of left-right asymmetry: a situs inversus mutation. Science 260: 679-682 (Pubitemid 23167591)
11. Yost HJ, (1991) Development of the left-right axis in amphibians. Ciba Found Symp 162: 165-176; discussion 176-181
12. Levin M, Johnson RL, Stern CD, Kuehn M, Tabin C, (1995) A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82: 803-814
13. Brown NA, Wolpert L, (1990) The development of handedness in left/right asymmetry. Development 109: 1-9
14. Speder P, Petzoldt A, Suzanne M, Noselli S, (2007) Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr Opin Genet Dev 17: 351-358 (Pubitemid 47238607)
15. Hirokawa N, Tanaka Y, Okada Y, Takeda S, (2006) Nodal flow and the generation of left-right asymmetry. Cell 125: 33-45
16. Vandenberg LN, Levin M, (2013) A unified model for left-right asymmetry? Comparison and synthesis of molecular models of embryonic laterality. Dev Biol 379: 1-15
17. Lee JD, Anderson KV, (2008) Morphogenesis of the node and notochord: the cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev Dyn 237: 3464-3476
18. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N, (1998) Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95: 829-837 (Pubitemid 29014462)
19. -/- mice analysis. J Cell Biol 145: 825-836 (Pubitemid 29240858)
20. Supp DM, Witte DP, Potter SS, Brueckner M, (1997) Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389: 963-966 (Pubitemid 27485686)
21. McGrath J, Somlo S, Makova S, Tian X, Brueckner M, (2003) Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114: 61-73 (Pubitemid 36859841)
22. Supp DM, Brueckner M, Kuehn MR, Witte DP, Lowe LA, McGrath J, Corrales J, Potter SS, (1999) Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 126: 5495-5504 (Pubitemid 30015941)
23. Okada Y, Nonaka S, Tanaka Y, Saijoh Y, Hamada H, Hirokawa N, (1999) Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol Cell 4: 459-468 (Pubitemid 29531126)
24. Kartagener H, (1935) Bronchiektasien bei situs viscerum inversus. Schweiz Med Wocshenschr 65: 782-784
25. Nonaka S, Shiratori H, Saijoh Y, Hamada H, (2002) Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418: 96-99 (Pubitemid 34742578)
26. Shinohara K, Kawasumi A, Takamatsu A, Yoshiba S, Botilde Y, Motoyama N, Reith W, Durand B, Shiratori H, Hamada H, (2012) Two rotating cilia in the node cavity are sufficient to break left-right symmetry in the mouse embryo. Nat Commun 3: 622
27. Nakamura T, Mine N, Nakaguchi E, Mochizuki A, Yamamoto M, Yashiro K, Meno C, Hamada H, (2006) Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev Cell 11: 495-504 (Pubitemid 44467724)
28. Sampaio P, Ferreira RR, Guerrero A, Pintado P, Tavares B, Amaro J, Smith AA, Montenegro-Johnson T, Smith DJ, Lopes SS, (2014) Left-right organizer flow dynamics: how much cilia activity reliably yields laterality? Dev Cell 29: 716-728
29. Brennan J, Norris DP, Robertson EJ, (2002) Nodal activity in the node governs left-right asymmetry. Genes Dev 16: 2339-2344 (Pubitemid 35034403)
30. Meno C, Shimono A, Saijoh Y, Yashiro K, Mochida K, Ohishi S, Noji S, Kondoh H, Hamada H, (1998) Lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94: 287-297 (Pubitemid 28376073)
31. Yamamoto M, Mine N, Mochida K, Sakai Y, Saijoh Y, Meno C, Hamada H, (2003) Nodal signaling induces the midline barrier by activating nodal expression in the lateral plate. Development 130: 1795-1804 (Pubitemid 36575907)
32. Logan M, Pagan-Westphal SM, Smith DM, Paganessi L, Tabin CJ, (1998) The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell 94: 307-317 (Pubitemid 28376075)
33. Piedra ME, Icardo JM, Albajar M, Rodriguez-Rey JC, Ros MA, (1998) Pitx2 participates in the late phase of the pathway controlling left-right asymmetry. Cell 94: 319-324 (Pubitemid 28376076)
34. Ryan AK, Blumberg B, Rodriguez-Esteban C, Yonei-Tamura S, Tamura K, Tsukui T, de la Peña J, Sabbagh W, Greenwald J, Choe S, et al, (1998) Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 394: 545-551 (Pubitemid 28366821)
35. Yoshioka H, Meno C, Koshiba K, Sugihara M, Itoh H, Ishimaru Y, Inoue T, Ohuchi H, Semina EV, Murray JC, et al, (1998) Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry. Cell 94: 299-305 (Pubitemid 28376074)
36. Okada Y, Takeda S, Tanaka Y, Izpisua Belmonte JC, Hirokawa N, (2005) Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121: 633-644 (Pubitemid 40720015)
37. Nonaka S, Yoshiba S, Watanabe D, Ikeuchi S, Goto T, Marshall WF, Hamada H, (2005) De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol 3: e268
38. Cartwright JH, Piro O, Tuval I, (2004) Fluid-dynamical basis of the embryonic development of left-right asymmetry in vertebrates. Proc Natl Acad Sci USA 101: 7234-7239 (Pubitemid 38638016)
39. Goodrich LV, Strutt D, (2011) Principles of planar polarity in animal development. Development 138: 1877-1892
40. Antic D, Stubbs JL, Suyama K, Kintner C, Scott MP, Axelrod JD, (2010) Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS ONE 5: e8999
41. Borovina A, Superina S, Voskas D, Ciruna B, (2010) Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat Cell Biol 12: 407-412
42. Hashimoto M, Shinohara K, Wang J, Ikeuchi S, Yoshiba S, Meno C, Nonaka S, Takada S, Hatta K, Wynshaw-Boris A, et al, (2010) Planar polarization of node cells determines the rotational axis of node cilia. Nat Cell Biol 12: 170-176
43. Song H, Hu J, Chen W, Elliott G, Andre P, Gao B, Yang Y, (2010) Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466: 378-382
44. Mahaffey JP, Grego-Bessa J, Liem KF Jr, Anderson KV, (2013) Cofilin and Vangl2 cooperate in the initiation of planar cell polarity in the mouse embryo. Development 140: 1262-1271
45. Norris DP, (2012) Cilia, calcium and the basis of left-right asymmetry. BMC Biol 10: 102
46. Tanaka Y, Okada Y, Hirokawa N, (2005) FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435: 172-177 (Pubitemid 40685936)
47. Field S, Riley KL, Grimes DT, Hilton H, Simon M, Powles-Glover N, Siggers P, Bogani D, Greenfield A, Norris DP, (2011) Pkd1l1 establishes left-right asymmetry and physically interacts with Pkd2. Development 138: 1131-1142
48. Pennekamp P, Karcher C, Fischer A, Schweickert A, Skryabin B, Horst J, Blum M, Dworniczak B, (2002) The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12: 938-943 (Pubitemid 34689231)
49. Yoshiba S, Shiratori H, Kuo IY, Kawasumi A, Shinohara K, Nonaka S, Asai Y, Sasaki G, Belo JA, Sasaki H, et al, (2012) Cilia at the node of mouse embryos sense fluid flow for left-right determination via Pkd2. Science 338: 226-231
50. Kamura K, Kobayashi D, Uehara Y, Koshida S, Iijima N, Kudo A, Yokoyama T, Takeda H, (2011) Pkd1l1 complexes with Pkd2 on motile cilia and functions to establish the left-right axis. Development 138: 1121-1129
51. Gardner RL, (2010) Normal bias in the direction of fetal rotation depends on blastomere composition during early cleavage in the mouse. PLoS ONE 5: e9610
52. Armakolas A, Klar AJ, (2007) Left-right dynein motor implicated in selective chromatid segregation in mouse cells. Science 315: 100-101 (Pubitemid 46196988)
53. Sauer S, Klar AJ, (2012) Left-right symmetry breaking in mice by left-right dynein may occur via a biased chromatid segregation mechanism, without directly involving the Nodal gene. Front Oncol 2: 166
54. Noel ES, Verhoeven M, Lagendijk AK, Tessadori F, Smith K, Choorapoikayil S, den Hertog J, Bakkers J, (2013) A Nodal-independent and tissue-intrinsic mechanism controls heart-looping chirality. Nat Commun 4: 2754
55. Feistel K, Blum M, (2006) Three types of cilia including a novel 9+4 axoneme on the notochordal plate of the rabbit embryo. Dev Dyn 235: 3348-3358 (Pubitemid 44888200)
56. Stephen LA, Johnson EJ, Davis GM, McTeir L, Pinkham J, Jaberi N, Davey MG, (2014) The chicken left right organizer has nonmotile cilia which are lost in a stage-dependent manner in the talpid ciliopathy. Genesis 52: 600-613
57. Cui C, Little CD, Rongish BJ, (2009) Rotation of organizer tissue contributes to left-right asymmetry. Anat Rec 292: 557-561
58. Gros J, Feistel K, Viebahn C, Blum M, Tabin CJ, (2009) Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 324: 941-944
59. +-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111: 77-89
60. +-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133: 1657-1671 (Pubitemid 43810973)
61. Aw S, Adams DS, Qiu D, Levin M, (2008) H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mech Dev 125: 353-372
62. Shimeld SM, Levin M, (2006) Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Dev Dyn 235: 1543-1553 (Pubitemid 43787956)
63. Nishide K, Mugitani M, Kumano G, Nishida H, (2012) Neurula rotation determines left-right asymmetry in ascidian tadpole larvae. Development 139: 1467-1475
64. Raff RA, Snoke Smith M, (2009) Chapter 7. Axis formation and the rapid evolutionary transformation of larval form. Curr Top Dev Biol 86: 163-190
65. Molina MD, de Croze N, Haillot E, Lepage T, (2013) Nodal: master and commander of the dorsal-ventral and left-right axes in the sea urchin embryo. Curr Opin Genet Dev 23: 445-453
66. Duboc V, Rottinger E, Lapraz F, Besnardeau L, Lepage T, (2005) Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev Cell 9: 147-158 (Pubitemid 40903667)
67. Frasnelli E, Vallortigara G, Rogers LJ, (2012) Left-right asymmetries of behaviour and nervous system in invertebrates. Neurosci Biobehav Rev 36: 1273-1291
68. Grande C, Patel NH, (2009) Nodal signalling is involved in left-right asymmetry in snails. Nature 457: 1007-1011
69. Shimizu K, Iijima M, Setiamarga DH, Sarashina I, Kudoh T, Asami T, Gittenberger E, Endo K, (2013) Left-right asymmetric expression of dpp in the mantle of gastropods correlates with asymmetric shell coiling. Evodevo 4: 15
70. Kuroda R, Endo B, Abe M, Shimizu M, (2009) Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails. Nature 462: 790-794
71. Shibazaki Y, Shimizu M, Kuroda R, (2004) Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo. Curr Biol 14: 1462-1467 (Pubitemid 39123743)
72. Liu MM, Davey JW, Banerjee R, Han J, Yang F, Aboobaker A, Blaxter ML, Davison A, (2013) Fine mapping of the pond snail left-right asymmetry (chirality) locus using RAD-Seq and fibre-FISH. PLoS ONE 8: e71067
73. Freeman G, Lundelius JW, (1982) The developmental genetics of dextrality and sinistrality in the gastropod Lymnaea peregra. Wilhelm Roux's Arc Dev Biol 191: 69-83
74. Ueshima R, Asami T, (2003) Evolution: single-gene speciation by left-right reversal. Nature 425: 679 (Pubitemid 37314303)
75. Hoso M, Kameda Y, Wu SP, Asami T, Kato M, Hori M, (2010) A speciation gene for left-right reversal in snails results in anti-predator adaptation. Nat Commun 1: 133
76. Pohl C, (2011) Left-right patterning in the C. elegans embryo: unique mechanisms and common principles. Commun Integr Biol 4: 34-40
77. Wood WB, (1998) Handed asymmetry in nematodes. Semin Cell Dev Biol 9: 53-60 (Pubitemid 128350417)
78. Hutter H, Schnabel R, (1995) Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: a multistep process involving a series of inductive events. Development 121: 3417-3424
79. Hutter H, Schnabel R, (1995) Specification of anterior-posterior differences within the AB lineage in the C. elegans embryo: a polarising induction. Development 121: 1559-1568
80. Pohl C, Bao Z, (2010) Chiral forces organize left-right patterning in C. elegans by uncoupling midline and anteroposterior axis. Dev Cell 19: 402-412
81. Bergmann DC, Lee M, Robertson B, Tsou MF, Rose LS, Wood WB, (2003) Embryonic handedness choice in C. elegans involves the Galpha protein GPA-16. Development 130: 5731-5740 (Pubitemid 37540847)
82. Johnston CA, Afshar K, Snyder JT, Tall GG, Gonczy P, Siderovski DP, Willard FS, (2008) Structural determinants underlying the temperature-sensitive nature of a Galpha mutant in asymmetric cell division of Caenorhabditis elegans. J Biol Chem 283: 21550-21558
83. Cabello J, Neukomm LJ, Gunesdogan U, Burkart K, Charette SJ, Lochnit G, Hengartner MO, Schnabel R, (2010) The Wnt pathway controls cell death engulfment, spindle orientation, and migration through CED-10/Rac. PLoS Biol 8: e1000297
84. Bischoff M, Schnabel R, (2006) A posterior centre establishes and maintains polarity of the Caenorhabditis elegans embryo by a Wnt-dependent relay mechanism. PLoS Biol 4: e396
85. Hermann GJ, Leung B, Priess JR, (2000) Left-right asymmetry in C. elegans intestine organogenesis involves a LIN-12/Notch signaling pathway. Development 127: 3429-3440
86. Wood WB, (1991) Evidence from reversal of handedness in C. elegans embryos for early cell interactions determining cell fates. Nature 349: 536-538 (Pubitemid 21912101)
87. Hobert O, Johnston RJ Jr, Chang S, (2002) Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat Rev Neurosci 3: 629-640 (Pubitemid 135706671)
88. Troemel ER, Sagasti A, Bargmann CI, (1999) Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99: 387-398
89. Poole RJ, Hobert O, (2006) Early embryonic programming of neuronal left/right asymmetry in C. elegans. Curr Biol 16: 2279-2292 (Pubitemid 44821833)
90. Bertrand V, Bisso P, Poole RJ, Hobert O, (2011) Notch-dependent induction of left/right asymmetry in C. elegans interneurons and motoneurons. Curr Biol 21: 1225-1231
91. Cochella L, Hobert O, (2012) Embryonic priming of a miRNA locus predetermines postmitotic neuronal left/right asymmetry in C. elegans. Cell 151: 1229-1242
92. Zhang F, O'Meara MM, Hobert O, (2011) A left/right asymmetric neuronal differentiation program is controlled by the Caenorhabditis elegans lsy-27 zinc-finger transcription factor. Genetics 188: 753-759
93. Coutelis JB, Geminard C, Speder P, Suzanne M, Petzoldt AG, Noselli S, (2013) Drosophila left/right asymmetry establishment is controlled by the Hox gene abdominal-B. Dev Cell 24: 89-97
94. Speder P, Adam G, Noselli S, (2006) Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 440: 803-807
95. Geminard C, Gonzalez-Morales N, Coutelis JB, Noselli S, (2014) The myosin ID pathway and left-right asymmetry in Drosophila. Genesis 52: 471-480
96. Coutelis JB, Petzoldt AG, Speder P, Suzanne M, Noselli S, (2008) Left-right asymmetry in Drosophila. Semin Cell Dev Biol 19: 252-262
97. Hozumi S, Maeda R, Taniguchi K, Kanai M, Shirakabe S, Sasamura T, Spéder P, Noselli S, Aigaki T, Murakami R, et al, (2006) An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 440: 798-802
98. Hozumi S, Maeda R, Taniguchi-Kanai M, Okumura T, Taniguchi K, Kawakatsu Y, Nakazawa N, Hatori R, Matsuno K, (2008) Head region of unconventional myosin I family members is responsible for the organ-specificity of their roles in left-right polarity in Drosophila. Dev Dyn 237: 3528-3537
99. Suzanne M, Petzoldt AG, Speder P, Coutelis JB, Steller H, Noselli S, (2010) Coupling of apoptosis and L/R patterning controls stepwise organ looping. Curr Biol 20: 1773-1778
100. Maeda RK, Karch F, (2009) The bithorax complex of Drosophila an exceptional Hox cluster. Curr Top Dev Biol 88: 1-33
101. Speder P, Noselli S, (2007) Left-right asymmetry: class I myosins show the direction. Curr Opin Cell Biol 19: 82-87 (Pubitemid 46123972)
102. Krendel M, Mooseker MS, (2005) Myosins: tails (and heads) of functional diversity. Physiology (Bethesda) 20: 239-251 (Pubitemid 41215198)
103. Nambiar R, McConnell RE, Tyska MJ, (2010) Myosin motor function: the ins and outs of actin-based membrane protrusions. Cell Mol Life Sci 67: 1239-1254
104. Barylko B, Binns DD, Albanesi JP, (2000) Regulation of the enzymatic and motor activities of myosin I. Biochim Biophys Acta 1496: 23-35 (Pubitemid 30155595)
105. Greenberg MJ, Ostap EM, (2013) Regulation and control of myosin-I by the motor and light chain-binding domains. Trends Cell Biol 23: 81-89
106. Hokanson DE, Laakso JM, Lin T, Sept D, Ostap EM, (2006) Myo1c binds phosphoinositides through a putative pleckstrin homology domain. Mol Biol Cell 17: 4856-4865 (Pubitemid 44665754)
107. Hokanson DE, Ostap EM, (2006) Myo1c binds tightly and specifically to phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate. Proc Natl Acad Sci USA 103: 3118-3123 (Pubitemid 43346434)
108. Taniguchi K, Maeda R, Ando T, Okumura T, Nakazawa N, Hatori R, Nakamura M, Hozumi S, Fujiwara H, Matsuno K, (2011) Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis. Science 333: 339-341
109. Petzoldt AG, Coutelis JB, Geminard C, Speder P, Suzanne M, Cerezo D, Noselli S, (2012) DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment. Development 139: 1874-1884
110. Chen TH, Hsu JJ, Zhao X, Guo C, Wong MN, Huang Y, Li Z, Garfinkel A, Ho CM, Tintut Y, et al, (2012) Left-right symmetry breaking in tissue morphogenesis via cytoskeletal mechanics. Circ Res 110: 551-559
111. Wan LQ, Ronaldson K, Park M, Taylor G, Zhang Y, Gimble JM, Vunjak-Novakovic G, (2011) Micropatterned mammalian cells exhibit phenotype-specific left-right asymmetry. Proc Natl Acad Sci USA 108: 12295-12300
112. Wan LQ, Vunjak-Novakovic G, (2011) Micropatterning chiral morphogenesis. Commun Integr Biol 4: 745-748
113. Xu J, Van Keymeulen A, Wakida NM, Carlton P, Berns MW, Bourne HR, (2007) Polarity reveals intrinsic cell chirality. Proc Natl Acad Sci USA 104: 9296-9300 (Pubitemid 47185773)
114. Pyrpassopoulos S, Feeser EA, Mazerik JN, Tyska MJ, Ostap EM, (2012) Membrane-bound myo1c powers asymmetric motility of actin filaments. Curr Biol 22: 1688-1692
115. Kim SV, Flavell RA, (2008) Myosin I: from yeast to human. Cell Mol Life Sci 65: 2128-2137
116. Richards TA, Cavalier-Smith T, (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436: 1113-1118 (Pubitemid 41232283)
117. Berg JS, Powell BC, Cheney RE, (2001) A millennial myosin census. Mol Biol Cell 12: 780-794 (Pubitemid 33051978)
118. Tzolovsky G, Millo H, Pathirana S, Wood T, Bownes M, (2002) Identification and phylogenetic analysis of Drosophila melanogaster myosins. Mol Biol Evol 19: 1041-1052 (Pubitemid 34743229)