Muscle precursor cells in the developing limbs of two isopods (Crustacea, Peracarida): An immunohistochemical study using a novel monoclonal antibody against myosin heavy chain

Development Genes and Evolution

Volumn 218, Issue 5, 2008, Pages 253-265

  Kreissl, S ^a   Uber, A ^a   Harzsch, S ^b  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Appendage; Crustacea; Evolution; Isopoda; Muscle precursor

Indexed keywords

MONOCLONAL ANTIBODY; MUSCLE PROTEIN; MYOSIN HEAVY CHAIN;

ANIMAL CELL; ANIMAL TISSUE; ARTHROPOD; ARTICLE; CONTROLLED STUDY; CRUSTACEA; EMBRYO; EMBRYO DEVELOPMENT; IDOTEA BALTHICA; IMMUNOHISTOCHEMISTRY; ISOPODA; LIMB DEVELOPMENT; MALACOSTRACA; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; PERACARIDA; PORCELLIO SCABER; PRIORITY JOURNAL; PROTEIN BINDING; SPECIES DIFFERENTIATION; STEM CELL; THORAX;

ANIMALS; ANTIBODIES, MONOCLONAL; EMBRYO, NONMAMMALIAN; EXTREMITIES; IMMUNOHISTOCHEMISTRY; ISOPODA; MUSCLE DEVELOPMENT; MUSCLES; MYOBLASTS; MYOSIN HEAVY CHAINS;

ANIMALIA; ARTHROPODA; CRUSTACEA; HEXAPODA; IDOTEA BALTICA; ISOPODA; MALACOSTRACA; PERACARIDA; PORCELLIO SCABER;

EID: 43049094382     PISSN: 0949944X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00427-008-0216-1     Document Type: Article

References (107)

1. Abmayr SM, Keller CA (1998) Drosophila myogenesis and insights into the role of nautilus. Curr Topics Dev Biol 38:35-80
2. Abzhanov A, Kaufman TC (1999) Novel regulation of the homeotic gene Scr associated with a crustacean leg-to-maxilliped appendage transformation. Development 126:1121-1128
3. Abzhanov A, Kaufmann TC (2000) Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227:673-689
4. Aigner S, Gohlsch B, Hamalainen N, Staron RS, Uber A, Wehrle U, Pette D (1993) Fast myosin heavy chain diversity in skeletal muscles of the rabbit: Heavy chain IId, not IIb predominates. Eur J Biochem 211:367-372
5. Akam M (1998a) The yin and yan of evo/devo. Cell 92:153-155
6. Akam M (1998b) Hox genes in arthropod development and evolution. Biol Bull 195:373-374
7. Alexander CG (1972) Locomotion in the isopod crustacean Ligia oceanica (Linn.). Comp Biochem Physiol 42A:1039-1047
8. Arcaro KF, Lnenicka GA (1995) Intrinsic differences in axonal growth from crayfish fast and slow motoneurons. Dev Biol 168:272-283
9. Averof M, Akam M (1995) Insect-crustacean relationships: Insights from comparative developmental and molecular studies. Philos Trans R Soc Lond B 347:293-303
10. Averof M, Dawes R, Ferrier D (1996) Diversification of arthropod /Hox/ genes as a paradigm for the evolution of gene functions. Semin Cell Dev Biol 7:539-551
11. Averof M, Cohen SM (1997) Evolutionary origin of insect wings from ancestral gills. Nature 385:627-630
12. Averof M, Patel NH (1997) Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388:682-686
13. Ball EE, Goodman CS (1985a) Muscle development in the grasshopper embryo II. Syncytial origin of the extensor tibiae muscle pioneers. Dev Biol 111:399-416
14. Ball EE, Goodman CS (1985b) Muscle development in the grasshopper embryo III. Sequential origin of the flexor tibiae muscle pioneers. Dev Biol 111:417-424
15. Ball EE, Ho RK, Goodman CS (1985) Muscle development in the grasshopper embryo I. Muscles, nerves, and apodemes in the metathoracic leg. Dev Biol 111:383-398
16. Baylies MK, Bate M, Gomez MR (1998) Myogenesis: A view from Drosophila. Cell 93:921-927
17. Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina. Zool Jb Anat 86:307-458
18. Bitsch J (2001) The hexapod appendage: Basic structure, development and origin. In: Deuve T (ed) Origin of the hexapoda. Ann Soc Entomol Fr (NS) 37:175-194
19. Boxshall GA (1985) The comparative anatomy of two copepods, a predatory calanoid and a particle-feeding mormoniloid. Philos Trans R Soc Lond B 311:303-377
20. Boxshall GA (1990) The skeletomusculature of siphonostomatoid copepods, with an analysis of adaptive radiation in structure of the oral cone. Philos Trans R Soc Lond B 328:167-212
21. Boxshall G (1997) Comparative limb morphology in major crustacean groups: The coxa-basis joint in postmandibular limbs. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman and Hall, London, pp 155-168
22. Brena C, Liu PZ, Minelli A, Kaufman TC (2005) Abd-B expression in PorcelCio scaber Latreille, 1804 (Isopoda: Crustacea): conserved pattern versus novel roles in development and evolution. Evol Dev 7:42-50
23. Browne WE, Patel NH (2000) Molecular genetics of crustacean feeding appendage development and diversification. Semin Cell Dev Biol 11:427-436
24. Brusca GJ (1981) On the anatomy of Cystisoma (Amphipoda: Hyperiidea). J Crust Biol 1:358-375
25. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer-Verlag, Berlin Heidelberg New York, p 405
26. Cattaert D, Le Ray D (2001) Adaptive motor control in crayfish. Prog Neurobiol 63:99-240
27. Clarac F (2002) Neurobiology of crustacean walking: From past to future. In: Wiese K (ed) Crustacean experimental systems in neurobiology. Springer-Verlag, Berlin Heidelberg New York, pp 119-140
28. Cole JC, Lang F (1980) Spontaneous and evoked postsynaptic potentials in an embryonic neuromuscular system of the lobster, Homarus americanus. J Neurobiol 11:459-470
29. Consoulas C, Levine RB (1997) Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation. J Neurobiol 1997:531-553
30. Consoulas C, Anezaki M, Levine RB (1997) Development of adult thoracic leg muscles during metamorphosis of the hawk moth Manduca sexta. Cell Tissue Res 287:393-412
31. Costello WJ, Hill R, Lang F (1981) Innervation patterns of fast and slow motor neurones during development of a lobster neuromuscular system. J Exp Biol 91:271-284
32. D'Albis A, Pantaloni C, Bechet J (1979) An electrophoretic study of native myosin isoenzymes and of their subunit content. Eur J Biochem 156:291-296
33. Davis WJ, Davis KB (1973) Ontogeny of a simple locomotor system: Role of the periphery in the development of central nervous circuitry. Am Zool 13:400-425
34. El Haj AJ (1999) Regulation of muscle growth and sarcomeric protein gene expression over the intermolt cycle. Amer Zool 39:570-579
35. Erhard F (1997) The pleonal skeleton and musculature of Titanethes albus (Synocheta) and of further taxa of the Oniscidea (Isopoda), with conclusion on the phylogeny of terrestrial isopods. Stuttgarter Beitr Naturk A 550:1-70
36. Evoy WH, Ayers J (1982) Locomotion and control of limb movements. In: Sandeman DC, Atwood HL (eds) The biology of Crustacea 4: Neural integration and behavior. Academic, New York, pp 62-106
37. Fryers G (1988) Studies on the functional morphology and biology of the Notostraca (Crustacea: Branchiopoda). Philos Trans R Soc Lond B 321:27-124
38. Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789-5801
39. Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357-372
40. Gonzàles-Crespo, Morata G (1996) Genetic evidence for the subdivision of the arthropod limb into coxopodite and telopodite. Development 122:3921-3928
41. Govind CK (1982) Development of nerve, muscle, and synapse. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea 3: Neurobiology: structure and function. Academic, New York, pp 185-205
42. Govind CK (1995) Muscles and their innervation. In: Factor IR (ed) Biology of the lobster. Academic, New York, pp 291-312
43. Govind CK (2002) Synapse specification for regenerated motoneurons in crayfish muscle. In: Wiese K (ed) Crustacean experimental systems in neurobiology. Springer-Verlag, Berlin Heidelberg New York, pp 175-188
44. Govind CK, Atwood (1982) Organization of neuromuscular systems. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea 3: Neurobiology: structure and function. Academic, New York, pp 63-104
45. Govind CK, Derosa RA (1983) Fine structure of comparable synapses in a mature and larval lobster muscle. Tissue Cell 15:97-106
46. Govind CK, Pearce J (1981) Remodeling of multiterminal innervation by nerve terminal sprouting in an identifiable lobster motoneuron. Science 212:1522-1524
47. Govind CK, Pearce J (1982) Proliferation and relocation of developing lobster neuromuscular synapses. Dev Biol 90:67-78
48. Govind CK, Pearce J (1989) Growth of inhibitory innervation in a lobster muscle. J Morphol 199:197-205
49. Govind CK, Walrond JP (1989) Structural plasticity at crustacean neuromuscular synapses. J Neurobiol 20:409-421
50. Govind CK, Meiss DE, Pearce J (1982) Differentiation of identifiable lobster neuromuscular synapses during development. J Neurocytol 11:235-247
51. Govind CK, Stephens PJ, Eisen JS (1985) Polyneuronal innervation of an adult and embryonic lobster muscle. J Embryol Exp Morph 87:13-26
52. Gruner HE (1954) Über das Coxalglied der Pereiopoden der Isopoden. Zool Anz 152:312-317
53. Harzsch S (2007) Architecture of the nervous system as a character for phylogenetic reconstructions: Examples from the Arthropoda. Species, Phylogeny, Evolution 1:33-57
54. Harzsch S, Hafner G (2006) Evolution of eye development in arthropods: phylogenetic implications. Arthropod Struct Dev 35:319-340
55. Hejnol A, Schnabel R, Scholtz G (2006) A 4D-microscopic analysis of the germ band in the isopod crustacean Porcellio scaber (Malacostraca, peracarida) - developmental and phylogenetic implications. Dev Genes Evol 216:755-767
56. Hertzler PL (2002) Development of the mesoderm in the dendrobrachiate shrimp Sycyonia ingentis. Arthropod Struct Dev 31:33-49
57. Hertzler PL (2005) Cleavage and gastrulation in the shrimp Penaeus (Litopenaeus) vannamei (Malacostraca, Decapoda, Dendrobranchiata. Arthropod Struct Dev 34:455-469
58. Hessler RD (1964) The Cephalocarida, comparative skeletomusculature. Mem Conn Acad Arts Sci 16:1-97
59. Ho RK, Ball EE, Goodman CS (1983) Muscle pioneers: Large mesodermal cells that erect a scaffold for developing muscles and motoneurones in grasshopper embryos. Nature 301:66-69
60. Hughes CL, Kaufman TC (2000) A diverse approach to arthropod development. Evol Dev 2:6-8
61. Kiernan DA, Hertzler PL (2006) Muscle development in dendrobranchiate shrimp, with comparison with Artemia. Evol Dev 8:537-549
62. Kirk MD, Govind CK (1992) Early innervation of abdominal swimmeret muscles in developing lobsters. J Exp Zool 261:298-309
63. Klass KD, Kristensen NP (2001) The ground plan and affinities of hexapods: Recent progress and open problems. In: Deuve T (ed) Origin of the Hexapoda. Ann Soc Entomol Fr (NS) 37:265-581
64. Kreissl S, Weiss T, Djokaj S, Balezina O, Rathmayer W (1999) Allatostatin modulates skeletal muscle performance in crustaceans through pre- and postsynaptic effects. Eur J Neurosci 11:2519-2530
65. Kukalova-Peck J (1997) Arthropod phylogeny and "basal"morphological structures. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman and Hall, London, pp 249-268
66. Lnenicka GA, Hong SJ, Combatti M, LePage S (1991) Activity-dependent development of synaptic varicosities at crayfish motor terminals. J Neurosci 11:1040-1048
67. Mellon De F Jr (1999) Muscle restructuring in crustaceans: Myofiber death, transfiguration and rebirth. Am Zool 39:527-540
68. Mykles DL (1999) Proteolytic processes underlying molt-induced claw muscle atrophy in decapod crustaceans. Am Zool 39:541-551
69. Nulsen C, Nagy LM (1999) The role of wingless in the development of multibranched crustacean limbs. Dev Genes Evol 209:340-348
70. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363-1366
71. Paululat A, Breuer S, Renkawitz-Pohl R (1999a) Determination and development of the larval muscle pattern in Drosophila melanogaster. Cell Tissue Res 296:151-160
72. Paululat A, Holz A, Renkawitz-Pohl R (1999b) Essential genes for myoblast fusion in Drosophila embryogenesis. Mech Dev 83:17-26
73. Pearce J, Govind CK, Meiss DE (1985) Growth-related features of lobster neuromuscular terminals. Dev Brain Res 21:215-228
74. Popadic A, Rusch D, Peterson M, Rogers BT, Kaufman TC (1996) Origin of the arthropod mandible. Nature 380:395
75. Popadic A, Panganiban G, Rusch D, Shear WA, Kaufman TC (1998) Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin on the labrum and other structures. Dev Genes Evol 208:142-150
76. Price AL, Patel NH (2008) Investigating divergent mechanisms of mesoderm development in Arthropods: The expression of Ph-twist and Ph-mef in Parhyale hawaiensis. J Exp Zool Mol Dev Evol 308B:24-40
77. Rathmayer W, Maier L (1986) Muscle fiber types in crabs: Studies on single identified muscle fibers. Amer Zool 27:1067-1077
78. Rathmayer W (1990) Inhibition through neurons of the common inhibitor type (CI-neurons) in crab muscles. In: Wiese K, Krenz WD, Tautz J, Reichert H, Mulloney B (eds) Frontiers in crustacean neurobiology. Birkhöäuser Verlag, Basel, pp 271-278, 7-190
79. Rathmayer W (2002) The study of neuromodulators-opening Pandora's box. In: Wiese K (ed) Crustacean experimental systems in neurobiology. Springer, Berlin, pp 165-168
80. Roy S, VijayRaghavan K (1999) Muscle pattern diversification in Drosophila: The story of imaginal myogenesis. BioEssays 21:486-498
81. Schmalfuss H (1974) Skelett und Extremitäten-Muskulatur des Isopoden Cephalotorax: Ein Beitrag zur Klärung von Phylogenie und Systematik der incertae-sedis-Familie Tylidae (Crustacea). Z Morph Tiere 78:1-91
82. Scholtz G, Mittman B, Gerberding M (1998) The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: New evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol 42:801-810
83. Schram FR, Koenemann S (2001) Developmental genetics and arthropod evolution: Part I, on legs. Evol Dev 3:343-354
84. Semmler H, Høeg JT, Scholtz G, Wanninger A (2006) Preliminary results on the anatomy of the larval musculature of Balanus improvisus (Darwin, 1854) (Crustacea: Cirripedia: Thecostraca) using phalloidin staining in combination with confocal laser scanning microscopy. Invertebr Reprod Dev 49:207-212
85. Steffens G, Xie F, Kutsch W, Reichert H (1995) Segmental differentiation processes in embryonic muscle development of the grasshopper. Roux's Arch Dev Biol 204:453-464
86. Stephens PJ, Govind CK (1981) Peripheral innervation fields of single lobster motoneurons defined by synapse elimination during development. Brain Res 212:476-480
87. Strömberg JO (1965) On the embryology of the isopod Idotea. Arkiv för Zoologi 15:421-473
88. Ungerer P, Wolff C (2005) External morphology of limb development in the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124:89-99
89. von Haffner K (1937) Untersuchungen über die ursprüngliche und abgeleitete Stellung der Beine bei den Isopoden. Zeitschr wiss Zool (Leipzig) 149:513-536
90. Wallay J (1969) Studies on the larval structure and metamosphosis of Balanus balanoides (L.). Philos Trans R Soc Lond B 256:183-279
91. Walossek D (1999) On the Cambrian diversity of Crustacea. In: Schram FR, von Vaupel Klein JC (eds) Crustaceans and the biodiversity crisis. Proceedings of the Fourth International Crustacean Congress. Brill, Leiden, Boston, Cologne, pp 3-27
92. Waloszek D (2003) Cambrian "Orsten"-type preserved arthropods and the phylogeny of Crustacea. Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) The new panorama of animal evolution. Proceedings of the 18th International Congress of Zoology, University of Athens, pp 69-87
93. Whitington PM, Leach D, Sandeman R (1993) Evolutionary change in neural development within the arthropods: Axogenesis in the embryos of two crustaceans. Development 118:449-461
94. Wiens (1989) Common and specific inhibition in leg muscles of decapods: sharpened distinctions. J Neurobiol 20:458-469
95. Wiens TJ, Wolf H (1993) The inhibitory motoneurons of crayfish thoracic limbs: Identification, structures, and homology with insect common inhibitors. J Comp Neurol 336:261-278
96. Wiersma CAG (1961) The neuromuscular system. In: Waterman TH (ed) The physiology of Crustacea II: Sense organs, integration, and behavior. Academic, New York, pp 191-240
97. Williams TA (1998) Distalless expression in crustaceans and the patterning of branched limbs. Dev Genes Evol 207:427-434
98. Williams TA (2004) The evolution and development of crustacean limbs: An analysis of limb homologies. Crustac Issues 15:169-196
99. Williams TA (2008) Early Distal-less expression in the developing crustacean limb bud becomes restricted to setal forming cells. Evol Dev 10:114-120
100. Williams TA, Müller GB (1996) Limb development in a primitive crustacean, Triops longicaudatus: Subdivision of the early limb bud gives rise to multibranched limbs. Dev Genes Evol 206:161-168
101. Williams TA, Nagy LM (1995) Brine shrimp add salt to the stew. Curr Biol 5:1330-1333
102. Williams TA, Nagy LM (1996) Comparative limb development in insects and crustaceans. Semin Cell Dev Biol 7:615-628
103. Williams TA, Nagy LM (2001) Developmental modularity and the evolutionary diversification of arthropod limbs. J Exp Zool (Mol Dev Evol) 291:241-257
104. Williams TA, Nulsen C, Nagy LM (2002) A complex role for distal-less in crustacean appendage development. Dev Biol 241:302-312
105. Wolf H, Harzsch S (2002) Evolution of the arthropod neuromuscular system: 1. Arrangement of muscles and excitatory innervation in the walking legs of the scorpion Vaejovis spinigerus (Wood, 1863) (Vaejovidae, Scorpiones, Arachnida). Arthropod Struct Dev 31:185-202
106. Xie F, Meier T, Reichert H (1992) Embryonic development of muscle patterns in the body wall of the grasshopper. Roux's Arch Dev Biol 201:301-311
107. Xie F, Garzino V, Therianos S, Meier T, Reichert H (1994) Embryonic expression of muscle-specific antigens in the grasshopper Schistocerca gregaria. Roux's Arch Dev Biol 204:141-145