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Is anisotropic propagation of polarized molecular distribution the common mechanism of swirling patterns of planar cell polarization? (English) Zbl 1400.92176

Summary: Mutations in multiple planar cell polarity (PCP) genes can cause swirling patterns indicated by whorls and tufts of hairs in the wings and the abdomen of Drosophila and in the skin of vertebrates. Damaged global directional cue caused by mutations in four-jointed, fat, and dachsous, impaired cellular hexagonal packing caused by mutations in frizzled, or weakened intracellular signaling caused by mutations in disheveled, inturned, and prickle all make hair patterns globally irregular yet locally aligned, and in some cases, typically swirling. Why and how mutations in different genes all lead to swirling patterns is unexplored. Although the mechanisms of molecular signaling remain unclear, the features of molecular distribution are evident – most PCP molecules develop the polarized distribution in cells and this distribution can be induced by intercellular signaling. Does this suggest something fundamental to swirling patterns beyond the particular functions of genes, proteins, and signaling? A simple model indeed indicates this. Disregarding detailed molecular interactions, the induced polarization of molecular distribution in an epithelial cell can be modeled as the induced polarization of positive and negative charge distribution in a dielectric molecule. Simulations reveal why and how mutations in different genes all lead to swirling patterns, and in particular, the conditions for generating typical swirling patterns. The results show that the anisotropic propagation of polarized molecular distribution may be the common mechanism of swirling patterns caused by different mutations. They also suggest that at the cell level, as at the molecular level, a simple mechanism can generate complex and diverse patterning phenotypes in different molecular contexts. The similarity between the induced polarization and its propagation in both the epithelial cells and the dielectric molecules also interestingly suggests some commonalities between pattern formation in the biological and physical systems.

MSC:

92C37 Cell biology
92C15 Developmental biology, pattern formation
35Q92 PDEs in connection with biology, chemistry and other natural sciences
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[1] Adler, P.N., Planar signaling and morphogenesis in drosophila, Dev. cell, 2, 525-535, (2002)
[2] Adler, P.N.; Krasnow, R.E.; Liu, J., Tissue polarity points from cells that have higher frizzled levels towards cells that have lower frizzled levels, Curr. biol., 7, 940-949, (1997)
[3] Adler, P.N.; Charlton, J.; Liu, J., Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling, Development, 125, 959-968, (1998)
[4] Affolter, M.; Mann, R., Legs, eyes, or wings—selectors and signals make the difference, Science, 292, 1080-1081, (2001)
[5] Amonlirdviman, K.; Khare, N.A.; Tree, D.R.P.; Chen, W.S.; Axelrod, J.D.; Tomlin, C.J., Mathematical modeling of planar cell polarity to understand domineering nonautonomy, Science, 307, 423-426, (2005)
[6] Benedek, G.B.; Villars, F.M.H., Physics with illustrative examples from medicine and biology – electricity and magnetism, (2000), Springer Berlin · Zbl 0963.92003
[7] Blankenship, J.T.; Backovic, S.T.; Sanny, J.S.P.; Weitz, O.; Zallen, J.A., Multicellular rosette formation links planar cell polarity to tissue morphogenesis, Dev. cell, 11, 459-470, (2006)
[8] Casal, J.; Struhl, G.; Lawrence, P.A., Developmental compartments and planar polarity in drosophila, Curr. biol., 12, 1189-1198, (2002)
[9] Cho, E.; Irvine, K.D., Action of fat, four-jointed, dachsous and dachsin distal-to-proximal wing signaling, Development, 131, 4489-4500, (2004)
[10] Classen, A.-K.; Anderson, K.I.; Marois, E.; Eaton, S., Hexagonal packing of drosophila wing epithelial cells by the planar cell polarity pathway, Dev. cell, 9, 805-817, (2005)
[11] Gubb, D.; Garcia-Bellido, A., A genetic analysis of the determination of cuticular polarity during development in drosophila melanogaster, J. embryol. exp. morphol., 68, 37-57, (1982)
[12] Keller, R., Shaping the vertebrate body plan by polarized embryonic cell movements, Science, 298, 1950-1954, (2002)
[13] Klein, T.J.; Mlodzik, M., Planar cell polarity: an emergent model points in the right direction, Annu. rev. cell dev. biol., 21, 155-176, (2005)
[14] Krasnow, R.E.; Wong, L.L.; Adler, P.N., Dishevelled is a component of the frizzled signaling pathway in drosophila, Development, 121, 4095-4102, (1995)
[15] Lawrence, P.A.; Casal, J.; Struhl, G., Cell interactions and planar polarity in the abdominal epidermis of drosophila, Development, 131, 4651-4664, (2004)
[16] Lawrence, P.A.; Struhl, G.; Casal, J., Planar cell polarity: one or two pathways?, Nat. rev. genet., 8, 555-563, (2007)
[17] Le Garrec, J.F.; Lopez, P.; Kerszberg, M., Establishment and maintenance of planar epithelial cell polarity by asymmetric cadherin bridges: a computer model, Dev. dyn., 235, 235-246, (2006)
[18] Lewis, J.; Davies, A., Planar cell polarity in the inner ear: how do hair cells acquire their oriented structure?, J. neurobiol., 53, 190-201, (2002)
[19] Ma, D.; Yang, C.; McNeill, H.; Simon, M.A.; Axelrod, J.D., Fidelity in planar cell polarity signaling, Nature, 421, 543-547, (2003)
[20] Matakatsu, H.; Blair, S.S., Interactions between fat and dachsous and the regulation of planar cell polarity in the drosophila wing, Development, 131, 3785-3794, (2004)
[21] Mlodzik, M., Planar cell polarization: do the same mechanisms regulate drosophila tissue polarity and vertebrate gastrulation?, Trends genet., 18, 564-571, (2002)
[22] Murray, J.D., Discussion: Turing theory of morphogenesis—its influence on modeling biological pattern and form, Bull. math. biol., 52, 119-152, (1990)
[23] Pertsov, A.M.; Davidenko, J.M.; Salomonsz, R.; Baxter, W.T.; Jalife, J., Spiral waves of excitation underlie reentrant activit in isolated cardiac muscle, Circ. res., 72, 631-650, (1993)
[24] Rawls, A.S.; Guinto, J.B.; Wolff, T., The cadherins fat and dachsous regulates dorsal/ventral signaling in the drosophila eye, Curr. biol., 12, 1021-1026, (2002)
[25] Shimada, Y.; Yonemura, S.; Ohkura, H.; Strutt, D.; Uemura, T., Polarized transport of frizzled along the planar microtubule arrays in drosophila wing epithelium, Dev. cell, 10, 209-222, (2006)
[26] Simon, M.A., Planar cell polarity in the drosophila eye is directed by graded four-jointed and dachsous expression, Development, 131, 6175-6184, (2004)
[27] Strutt, H.; Strutt, D., Nonautonomous planar polarity patterning in drosophila: dishevelled-independent functions of frizzled, Dev. cell, 3, 851-863, (2002)
[28] Strutt, D.; Strutt, H., Differential activities of the core planar polarity proteins during drosophila wing patterning, Dev. biol., 302, 181-194, (2007)
[29] Tayler, J.; Abramova, N.; Charlton, J.; Adler, P.N., Van gogh: a new drosophila tissue polarity gene, Genetics, 150, 199-210, (1998)
[30] Tree, D.R.P.; Ma, D.; Axelrod, J.D., A three-tiered mechanism for regulation of planar cell polarity, Sem. cell dev. biol., 13, 217-224, (2002)
[31] Tree, D.R.P.; Shulman, J.M.; Rousset, R.; Scott, M.P.; Gubb, D.; Axelrod, J.D., Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling, Cell, 109, 371-381, (2002)
[32] Usui, T.; Shima, Y.; Shimada, Y.; Hirano, S.; Burgess, R.W.; Schwarz, T.L.; Takeichi, M.; Uemura, T., Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of frizzled, Cell, 98, 585-595, (1999)
[33] Vinson, C.R.; Adler, P.N., Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of drosophila, Nature, 329, 549-551, (1987)
[34] Vinson, C.R.; Conover, S.; Adler, N., A drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains, Nature, 338, 263-264, (1989)
[35] Wallingford, J.B.; Rowning, B.A.; Vogeli, K.M.; Rothbacher, U.; Fraser, S.E.; Harland, R.M., Dishevelled controls cell polarity during xenopus gastrulation, Nature, 405, 81-85, (2000)
[36] Wang, Y.; Badea, T.; Nathans, J., Order from dis-order: self-organization in Mammalian hair patterning, Proc. natl. acad sci., 103, 19800-19805, (2006)
[37] Wehrli, M.; Tomlinson, A., Epithelial planar polarity in the developing drosophila eye, Development, 121, 2451-2459, (1995)
[38] Wong, L.L.; Adler, P.N., Tissue polarity genes of drosophila regulate the subcellular location for prehair initiation in pupal wing cells, J. cell biol., 123, 209-221, (1993)
[39] Yang, C.; Axelrod, J.D.; Simon, M., Regulation of frizzled by fat-like cadherins during planar polarity signaling in the drosophila compound eye, Cell, 108, 675-688, (2002)
[40] Zallen, J.A., Planar polarity and tissue morphogenesis, Cell, 129, 1051-1063, (2007)
[41] Zallen, J.A.; Wieschaus, E., Patterned gene expression directs bipolar planar polarity in drosophila, Dev. cell, 6, 343-355, (2004)
[42] Zeidler, M.P.; Perrimon, N.; Strutt, D.I., The four-jointed gene is required in the drosophila eye for ommatidial polarity specification, Curr. biol., 9, 1363-1372, (1999)
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