Hox genes and the regulation of movement in Drosophila

Many animals show regionally specialized patterns of movement along the body axis. In vertebrates, spinal networks regulate locomotion, while the brainstem controls movements of respiration and feeding. Similarly, amongst invertebrates diversification of appendages along the body axis is tied to the performance of characteristically different movements such as those required for feeding, locomotion, and respiration. Such movements require locally specialized networks of nerves and muscles. Here we use the regionally differentiated movements of larval crawling in Drosophila to investigate how the formation of a locally specialized locomotor network is genetically determined. By loss and gain of function experiments we show that particular Hox gene functions are necessary and sufficient to dictate the formation of a neuromuscular network that orchestrates the movements of peristaltic locomotion. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2008

[1]  H. Reichert,et al.  Homeotic gene action in embryonic brain development of Drosophila. , 1998, Development.

[2]  R. Harris-Warrick,et al.  The evolution of neuronal circuits underlying species-specific behavior , 1999, Current Opinion in Neurobiology.

[3]  V. Hamburger,et al.  Motility in chick embryos with substitution of lumbosacral by brachial and brachial by lumbosacral spinal cord segments. , 1971, The Journal of experimental zoology.

[4]  R J Full,et al.  How animals move: an integrative view. , 2000, Science.

[5]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[6]  Barry J. Dickson,et al.  fruitless Splicing Specifies Male Courtship Behavior in Drosophila , 2005, Cell.

[7]  R. Wingate,et al.  Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. , 1999, Science.

[8]  Andrew Lumsden,et al.  Patterning the Vertebrate Neuraxis , 1996, Science.

[9]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[10]  E. Sánchez-Herrero,et al.  Developmental consequences of unrestricted expression of the abd-A gene of Drosophila , 1994, Mechanisms of Development.

[11]  E. Lewis.  A gene complex controlling segmentation in Drosophila , 1978, Nature.

[12]  W. McGinnis,et al.  Activity regulation of Hox proteins, a mechanism for altering functional specificity in development and evolution. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[13]  D. M. Wilson.  Inherent asymmetry and reflex modulation of the locust flight motor pattern. , 1968, The Journal of experimental biology.

[14]  J. C. Hombría,et al.  Beyond homeosis--HOX function in morphogenesis and organogenesis. , 2003, Differentiation; research in biological diversity.

[15]  Jeffrey C. Hall,et al.  Are Complex Behaviors Specified by Dedicated Regulatory Genes? Reasoning from Drosophila , 2001, Cell.

[16]  B Mulloney,et al.  A separate local pattern-generating circuit controls the movements of each swimmeret in crayfish. , 1993, Journal of neurophysiology.

[17]  P. Bräunig,et al.  Insect mouthpart motor patterns: central circuits modified for highly derived appendages? , 2001, Neuroscience.

[18]  G. Morata,et al.  Functional and regulatory interactions between Hox and extradenticle genes. , 1998, Genes & development.

[19]  P. Callaerts,et al.  Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. , 1995, Science.

[20]  G. Technau,et al.  Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[21]  A. Michelson,et al.  Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. , 1994, Development.

[22]  Thomas M. Jessell,et al.  Motor neuron columnar fate imposed by sequential phases of Hox-c activity , 2003, Nature.

[23]  C Cremer,et al.  A fate map for the larval epidermis of Drosophila melanogaster: localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. , 1979, Developmental biology.

[24]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[25]  M. Akam,et al.  The molecular basis for metameric pattern in the Drosophila embryo. , 1987, Development.

[26]  V. Hartenstein,et al.  The emergence of patterned movement during late embryogenesis of Drosophila , 2007, Developmental neurobiology.

[27]  S. Grillner.  The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[28]  Thomas M. Jessell,et al.  A Hox Regulatory Network Establishes Motor Neuron Pool Identity and Target-Muscle Connectivity , 2005, Cell.

[29]  V. Hamburger,et al.  Motility in chick embryos with substitution of lumbosacral by brachial by lumbosacral spinal cord segments , 1971 .

[30]  M. Bastiani,et al.  From grasshopper to Drosophila: a common plan for neuronal development , 1984, Nature.

[31]  M. Scott,et al.  Distinct hox protein sequences determine specificity in different tissues. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Bate,et al.  Embryonic Origins of a Motor System:Motor Dendrites Form a Myotopic Mapin Drosophila , 2003, PLoS biology.

[33]  I. Miguel-Aliaga,et al.  Segment-specific prevention of pioneer neuron apoptosis by cell-autonomous, postmitotic Hox gene activity , 2004, Development.

[34]  C. Rieder,et al.  Greatwall kinase , 2004, The Journal of cell biology.