Histochemistry and Cell Biology

, Volume 142, Issue 5, pp 473–488 | Cite as

Retrograde migration of pectoral girdle muscle precursors depends on CXCR4/SDF-1 signaling

  • Maryna Masyuk
  • Aisha Abduelmula
  • Gabriela Morosan-Puopolo
  • Veysel Ödemis
  • Rizwan Rehimi
  • Nargis Khalida
  • Faisal Yusuf
  • Jürgen Engele
  • Hirokazu Tamamura
  • Carsten Theiss
  • Beate Brand-SaberiEmail author
Original Paper


In vertebrates, muscles of the pectoral girdle connect the forelimbs with the thorax. During development, the myogenic precursor cells migrate from the somites into the limb buds. Whereas most of the myogenic precursors remain in the limb bud to form the forelimb muscles, several cells migrate back toward the trunk to give rise to the superficial pectoral girdle muscles, such as the large pectoral muscle, the latissimus dorsi and the deltoid. Recently, this developing mode has been referred to as the “In–Out” mechanism. The present study focuses on the mechanisms of the “In–Out” migration during formation of the pectoral girdle muscles. Combining in ovo electroporation, tissue slice-cultures and confocal laser scanning microscopy, we visualize live in detail the retrograde migration of myogenic precursors from the forelimb bud into the trunk region by live imaging. Furthermore, we present for the first time evidence for the involvement of the chemokine receptor CXCR4 and its ligand SDF-1 during these processes. After microsurgical implantations of CXCR4 inhibitor beads in the proximal forelimb region of chicken embryos, we demonstrate with the aid of in situ hybridization and live-cell imaging that CXCR4/SDF-1 signaling is crucial for the retrograde migration of pectoral girdle muscle precursors. Moreover, we analyzed the MyoD expression in CXCR4-mutant mouse embryos and observed a considerable decrease in pectoral girdle musculature. We thus demonstrate the importance of the CXCR4/SDF-1 axis for the pectoral girdle muscle formation in avians and mammals.


Pectoral girdle muscles CXCR4/SDF-1 Time-lapse imaging Secondary trunk muscles In ovo electroporation 



The authors thank Prof. Dr. Ruijin Huang. M. Masyuk especially thanks FoRUM (RUB) for financial support by providing a dissertation scholarship. The authors further acknowledge S. Wulf, R. Houmany, and especially A. Lodwig for excellent technical assistance as well as A. Lenz and A. Conrad for secretarial work. This work was supported by MYORES project (511978) funded by the EU´s Sixth Framework Programme.

Supplementary material

418_2014_1237_MOESM1_ESM.tif (6 mb)
Fig. S1. CXCR4 inhibitor TN14003 does not cause cell death. CXCR4-inhibitor-soaked beads were implanted in the dorsal proximal forelimb region of HH23 chicken embryos. After reincubation up to stage HH26, TUNEL assay on transverse sections through the forelimb region was performed. (A,B) No increased apoptosis was discernible in the area around the CXCR4 inhibitor bead, while single physiologically apoptotic cells (red) were detectable in various locations of the specimen. (C,D) Tissue sections treated with bovine pancreas DNase I that cleaves the DNA-revealed apoptotic cells (red) over the entire specimen. (B,D) are higher magnification views of the bead areas in (A,C). Scale bars: 100 µm. (TIFF 6132 kb)

Movie 1. Live-cell imaging of the retrograde migration during the retrograde migration of pectoral girdle muscle precursors. The movie relates to Fig. 2. Using in ovo electroporation of the ventrolateral dermomyotome of HH14 chicken embryos, premyogenic precursor cells were labeled with Tol2-EGFP construct. After reincubation up to stage HH26, slice cultures of the forelimb region were prepared. With the aid of confocal laser scanning microscopy, time-lapse movies that capture the retrograde migration of myogenic precursors from the forelimb bud toward the trunk were recorded. The myogenic precursor cells (green) are not restricted to the forelimb bud, but two groups of EGFP-labeled precursors are also visible in the dorsal and ventral pectoral girdle region, respectively. Individual cells actively migrate from the forelimb bud toward the trunk. This retrograde migration represents the “Out”-phase of the “In–Out” mechanism deployed during formation of pectoral girdle muscles. During monitoring the cells reveal a high proliferation rate. Scale bar: 100 µm. (MP4 2426 kb)

Movie 2. CXCR4 inhibitor TN14003 affects the retrograde migration of pectoral girdle muscle precursors. The movie relates to Fig. 5. Using in ovo electroporation of the ventrolateral dermomyotome of HH14 chicken embryos, premyogenic precursor cells were labeled with Tol2-EGFP construct. After reincubation up to stage HH23, acrylic beads soaked in CXCR4 inhibitor TN14003 were implanted into the dorsal proximal forelimb. After reincubation up to stage HH26, slice cultures of the forelimb region were prepared. With the aid of confocal laser scanning microscopy, time-lapse movies were recorded. The myogenic precursor cells (green) are visible in the dorsal and ventral forelimb region. The EGFP-labeled myogenic precursors in the dorsal forelimb show highly intensive movements during the entire recording period, but do not succeed in penetrating the area with the CXCR4 inhibitor solution. The retrograde migration of myogenic precursors required for the formation of pectoral girdle muscles is thus affected by the CXCR4 inhibitor TN14003. Scale bar: 100 µm. (MP4 2693 kb)

Movie 3. The acrylic bead does not mechanically affect the retrograde migration of pectoral girdle muscle precursors. The movie relates to Fig. 6. Using in ovo electroporation of the ventrolateral dermomyotome of HH14 chicken embryos, premyogenic precursor cells were labeled with Tol2-EGFP construct. After reincubation up to stage HH23, acrylic beads soaked in CXCR4 inhibitor TN14003 were implanted into the dorsal proximal forelimb. After reincubation up to stage HH26, slice cultures of the forelimb region were prepared. With the aid of confocal laser scanning microscopy, time-lapse movies were recorded. The myogenic precursor cells (green) are visible in the dorsal and ventral forelimb region. During the entire monitoring period, the EGFP-labeled myogenic precursors in the vicinity of the PBS-soaked acrylic bead reveal active motility. We can observe an individual progenitor cell actively migrating in the retrograde migration toward the trunk and passing across the PBS bead without any difficulties. Thus, the acrylic bead does not present a mechanical obstacle for the retrograde migration of the myogenic precursor cell. Scale bar: 100 µm. (MP4 2304 kb)

Movie 4. Tol2-EGFP-transfected cells are not affected by electroporation. The ventrolateral dermomyotome of HH14 chicken embryos was transfected with the Tol2-EGFP construct using electroporation. After three days of reincubation, slice cultures of the forelimb region were prepared. After another four days of reincubation, a movie was recorded using a fluorescent microscope. Contractile and viable EGFP-labeled fibers are detectable, demonstrating that the physiological development of myogenic precursor cells is not adversely affected by in ovo electroporation technique. (MP4 2393 kb)


  1. Baban A, Torre M, Bianca S, Buluggiu A, Rossello MI, Calevo MG, Valle M, Ravazzolo R, Jasonni V, Lerone M (2009) Poland syndrome with bilateral features: case description with review of the literature. Am J Med Genet A 149A(7):1597–1602PubMedCrossRefGoogle Scholar
  2. Balkwill F (2004) The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol 14(3):171–179PubMedCrossRefGoogle Scholar
  3. Bavinck JN, Weaver DD (1986) Subclavian artery supply disruption sequence: hypothesis of a vascular etiology for Poland, Klippel-Feil, and Möbius anomalies. Am J Med Genet 23(4):903–918PubMedCrossRefGoogle Scholar
  4. Ben-Yair R, Kalcheim C (2005) Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132(4):689–701PubMedCrossRefGoogle Scholar
  5. Ben-Yair R, Kalcheim C (2008) Notch and bone morphogenetic protein differentially act on dermomyotome cells to generate endothelium, smooth, and striated muscle. J Cell Biol 180(3):607–618PubMedCrossRefPubMedCentralGoogle Scholar
  6. Ben-Yair R, Kahane N, Kalcheim C (2003) Coherent development of dermomyotome and dermis from the entire mediolateral extent of the dorsal somite. Development 130(18):4325–4336PubMedCrossRefGoogle Scholar
  7. Beresford B (1983) Brachial muscles in the chick embryo: the fate of individual somites. J Embryol Exp Morphol 77:99–116PubMedGoogle Scholar
  8. Beresford B, Le Lievre C, Rathbone MP (1978) Chimaera studies of the origin and formation of the pectoral musculature of the avian embryo. J Exp Zool 205(2):321–326PubMedCrossRefGoogle Scholar
  9. Bergman RA, Thompson SA, Saadeh FA (1988) Anomalous fascicle and high origin of latissimus dorsi compensating for absence of serratus anterior. Anat Anz 167(2):161–164PubMedGoogle Scholar
  10. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376(6543):768–771PubMedCrossRefGoogle Scholar
  11. Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA (1996) A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 184(3):1101–1109PubMedCrossRefGoogle Scholar
  12. Bober E, Franz T, Arnold HH, Gruss P, Tremblay P (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120(3):603–612PubMedGoogle Scholar
  13. Brand-Saberi B, Wilting J, Ebensperger C, Christ B (1996) The formation of somite compartments in the avian embryo. Int J Dev Biol 40(1):411–420PubMedGoogle Scholar
  14. Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41:245–258PubMedGoogle Scholar
  15. Christ B, Brand-Saberi B (2002) Limb muscle development. Int J Dev Biol 46(7):905–914PubMedGoogle Scholar
  16. Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol 191(5):381–396PubMedCrossRefGoogle Scholar
  17. Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150(2):171–186PubMedCrossRefGoogle Scholar
  18. David TJ, Winter RM (1985) Familial absence of the pectoralis major, serratus anterior, and latissimus dorsi muscles. J Med Genet 22(5):390–392PubMedCrossRefPubMedCentralGoogle Scholar
  19. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, Di Marzio P, Marmon S, Sutton RE, Hill CM, Davis CB, Peiper SC, Schall TJ, Littman DR, Landau NR (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381(6584):661–666PubMedCrossRefGoogle Scholar
  20. Dietrich S, Abou-Rebyeh F, Brohmann H, Bladt F, Sonnenberg-Riethmacher E, Yamaai T, Lumsden A, Brand-Saberi B, Birchmeier C (1999) The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126(8):1621–1629PubMedGoogle Scholar
  21. Doitsidou M, Reichman-Fried M, Stebler J, Köprunner M, Dörries J, Meyer D, Esguerra CV, Leung T, Raz E (2002) Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111(5):647–659PubMedCrossRefGoogle Scholar
  22. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW (1996) A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85(7):1149–1158PubMedCrossRefGoogle Scholar
  23. Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272(5263):872–877PubMedCrossRefGoogle Scholar
  24. Franz T, Kothary R, Surani MA, Halata Z, Grim M (1993) The Splotch mutation interferes with muscle development in the limbs. Anat Embryol 187(2):153–160PubMedCrossRefGoogle Scholar
  25. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119(3):493–501PubMedCrossRefGoogle Scholar
  26. Grim M (1971) Development of the primordia of the latissimus dorsi muscle of the chicken. Folia Morphol 19(3):252–258Google Scholar
  27. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:1CrossRefGoogle Scholar
  28. Hegde HR, Shokeir MH (1982) Posterior shoulder girdle abnormalities with absence of pectoralis major muscle. Am J Med Genet 13(3):285–293PubMedCrossRefGoogle Scholar
  29. Hiratsuka S, Duda DG, Huang Y, Goel S, Sugiyama T, Nagasawa T, Fukumura D, Jain RK (2011) C-X-C receptor type 4 promotes metastasis by activating p38 mitogen-activated protein kinase in myeloid differentiation antigen (Gr-1)-positive cells. Proc Natl Acad Sci USA 108(1):302–307PubMedCrossRefPubMedCentralGoogle Scholar
  30. Huang R, Christ B (2000) Origin of the epaxial and hypaxial myotome in avian embryos. Anat Embryol 202(5):369–374PubMedCrossRefGoogle Scholar
  31. Jones HW (1926) Congenital absence of the pectoral muscles. Br Med J 6:59–60CrossRefGoogle Scholar
  32. Kalcheim C, Cinnamon Y, Kahane N (1999) Myotome formation: a multistage process. Cell Tissue Res 296(1):161–173PubMedCrossRefGoogle Scholar
  33. Kawakami K (2007) Tol2: a versatile gene transfer vector in vertebrates. Genome Biol 8(Suppl 1):S7PubMedCrossRefPubMedCentralGoogle Scholar
  34. Kawakami K, Shima A, Kawakami N (2000) Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc Natl Acad Sci USA 97(21):11403–11408PubMedCrossRefPubMedCentralGoogle Scholar
  35. Knaut H, Werz C, Geisler R, Nüsslein-Volhard C, Tübingen 2000 Screen Consortium (2003) A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421(6920):279–282PubMedCrossRefGoogle Scholar
  36. Koga A, Suzuki M, Inagaki H, Bessho Y, Hori H (1996) Transposable element in fish. Nature 383(6595):30PubMedCrossRefGoogle Scholar
  37. Krull CE (2004) A primer on using in ovo electroporation to analyze gene function. Dev Dyn 229(3):433–439PubMedCrossRefGoogle Scholar
  38. Lanser ME, Fallon JF (1987) Development of wing-bud-derived muscles in normal and wingless chick embryos: a computer-assisted three-dimensional reconstruction study of muscle pattern formation in the absence of skeletal elements. Anat Rec 217(1):61–78PubMedCrossRefGoogle Scholar
  39. Lazarini F, Tham TN, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M (2003) Role of the alpha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42(2):139–148PubMedCrossRefGoogle Scholar
  40. Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA 95(16):9448–9453PubMedCrossRefPubMedCentralGoogle Scholar
  41. Mansouri A, Hallonet M, Gruss P (1996) Pax genes and their roles in cell differentiation and development. Curr Opin Cell Biol 8(6):851–857PubMedCrossRefGoogle Scholar
  42. Marcelle C, Wolf J, Bronner-Fraser M (1995) The in vivo expression of the FGF receptor FREK mRNA in avian myoblasts suggests a role in muscle growth and differentiation. Dev Biol 172(1):100–114PubMedCrossRefGoogle Scholar
  43. Masyuk M, Morosan-Puopolo G, Brand-Saberi B, Theiss C (2014) Combination of in ovo electroporation and time-lapse imaging to study migrational events in chicken embryos. Dev Dyn 243(5):690–698PubMedCrossRefGoogle Scholar
  44. Mauger A (1972a) The role of somitic mesoderm in the development of dorsal plumage in chick embryos. I. Origin, regulative capacity and determination of the plumage-forming mesoderm. J Embryol Exp Morphol 28(2):313–341 (article in French)PubMedGoogle Scholar
  45. Mauger A (1972b) The role of somitic mesoderm in the development of dorsal plumage in chick embryos. II. Regionalization of the plumage-forming mesoderm. J Embryol Exp Morphol 28(2):343–366 (article in French)PubMedGoogle Scholar
  46. Morosan-Puopolo G, Balakrishnan-Renuka A, Yusuf F, Chen J, Dai F, Zoidl G, Lüdtke TH, Kispert A, Theiss C, Abdelsabour-Khalaf M, Brand-Saberi B (2014) Wnt11 is required for oriented migration of dermogenic progenitor cells from the dorsomedial lip of the avian dermomyotome. PLoS ONE 9(3):e92679PubMedCrossRefPubMedCentralGoogle Scholar
  47. Mosconi T, Kamath S (2003) Bilateral asymmetric deficiency of the pectoralis major muscle. Clin Anat 16(4):346–349PubMedCrossRefGoogle Scholar
  48. Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50–56PubMedCrossRefGoogle Scholar
  49. Nagashima H, Sugahara F, Takechi M, Ericsson R, Kawashima-Ohya Y, Narita Y, Kuratani S (2009) Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325(5937):193–196PubMedCrossRefGoogle Scholar
  50. Nieto MA, Patel K, Wilkinson DG (1996) In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219–235PubMedCrossRefGoogle Scholar
  51. Olivera-Martinez I, Coltey M, Dhouailly D, Pourquié O (2000) Mediolateral somitic origin of ribs and dermis determined by quail-chick chimeras. Development 127(21):4611–4617PubMedGoogle Scholar
  52. Olivera-Martinez I, Missier S, Fraboulet S, Thélu J, Dhouailly D (2002) Differential regulation of the chick dorsal thoracic dermal progenitors from the medial dermomyotome. Development 129(20):4763–4772PubMedGoogle Scholar
  53. Olivera-Martinez I, Thélu J, Dhouailly D (2004) Molecular mechanisms controlling dorsal dermis generation from the somitic dermomyotome. Int J Dev Biol 48(2–3):93–101PubMedCrossRefGoogle Scholar
  54. Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114(2):339–353PubMedGoogle Scholar
  55. Ott MO, Bober E, Lyons G, Arnold H, Buckingham M (1991) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111(4):1097–1107PubMedGoogle Scholar
  56. Paraskevas GK, Raikos A (2010) Bilateral pectoral musculature malformations with concomitant vascular anomaly. Folia Morphol 69(3):187–191Google Scholar
  57. Poland A (1841) Deficiency of the pectoral muscles. Guys Hosp Rep 6:191–193Google Scholar
  58. Pownall ME, Emerson CP Jr (1992) Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev Biol 151(1):67–79PubMedCrossRefGoogle Scholar
  59. Pu Q, Abduelmula A, Masyuk M, Theiss C, Schwandulla D, Hans M, Patel K, Brand-Saberi B, Huang R (2013) The dermomyotome ventrolateral lip is essential for the hypaxial myotome formation. BMC Dev Biol 13:37PubMedCrossRefPubMedCentralGoogle Scholar
  60. Pujol F, Kitabgi P, Boudin H (2005) The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons. J Cell Sci 118(Pt 5):1071–1080PubMedCrossRefGoogle Scholar
  61. Rehimi R, Khalida N, Yusuf F, Dai F, Morosan-Puopolo G, Brand-Saberi B (2008) Stromal-derived factor-1 (SDF-1) expression during early chick development. Int J Dev Biol 52(1):87–92PubMedCrossRefGoogle Scholar
  62. Rehimi R, Khalida N, Yusuf F, Morosan-Puopolo G, Brand-Saberi B (2010) A novel role of CXCR4 and SDF-1 during migration of cloacal muscle precursors. Dev Dyn 239(6):1622–1631PubMedCrossRefGoogle Scholar
  63. Sassoon DA (1993) Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev Biol 156(1):11–23PubMedCrossRefGoogle Scholar
  64. Sato Y, Kasai T, Nakagawa S, Tanabe K, Watanabe T, Kawakami K, Takahashi Y (2007) Stable integration and conditional expression of electroporated transgenes in chicken embryos. Dev Biol 305(2):616–624PubMedCrossRefGoogle Scholar
  65. Stebler J, Spieler D, Slanchev K, Molyneaux KA, Richter U, Cojocaru V, Tarabykin V, Wylie C, Kessel M, Raz E (2004) Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev Biol 272(2):351–361PubMedCrossRefGoogle Scholar
  66. Sullivan GE (1962) Anatomy and embryology of the wing musculature of the domestic fowl (Gallus). Aust J Zool 10:458–516CrossRefGoogle Scholar
  67. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89(1):127–138PubMedCrossRefGoogle Scholar
  68. Tamamura H, Xu Y, Hattori T, Zhang X, Arakaki R, Kanbara K, Omagari A, Otaka A, Ibuka T, Yamamoto N, Nakashima H, Fujii N (1998) A low-molecular-weight inhibitor against the chemokine receptor CXCR4: a strong anti-HIV peptide T140. Biochem Biophys Res Commun 253(3):877–882PubMedCrossRefGoogle Scholar
  69. Tamamura H, Omagari A, Hiramatsu K, Gotoh K, Kanamoto T, Xu Y, Kodama E, Matsuoka M, Hattori T, Yamamoto N, Nakashima H, Otaka A, Fujii N (2001) Development of specific CXCR4 inhibitors possessing high selectivity indexes as well as complete stability in serum based on an anti-HIV peptide T140. Bioorg Med Chem Lett 11(14):1897–1902PubMedCrossRefGoogle Scholar
  70. Valasek P, Evans DJ, Maina F, Grim M, Patel K (2005) A dual fate of the hindlimb muscle mass: cloacal/perineal musculature develops from leg muscle cells. Development 132(3):447–458PubMedCrossRefGoogle Scholar
  71. Valasek P, Theis S, DeLaurier A, Hinits Y, Luke GN, Otto AM, Minchin J, He L, Christ B, Brooks G, Sang H, Evans DJ, Logan M, Huang R, Patel K (2011) Cellular and molecular investigations into the development of the pectoral girdle. Dev Biol 357(1):108–116PubMedCrossRefGoogle Scholar
  72. Vasyutina E, Birchmeier C (2006) The development of migrating muscle precursor cells. Anat Embryol 211(Suppl 1):37–41PubMedGoogle Scholar
  73. Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C (2005) CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev 19(18):2187–2198PubMedCrossRefPubMedCentralGoogle Scholar
  74. Wilting J, Brand-Saberi B, Huang R, Zhi Q, Köntges G, Ordahl CP, Christ B (1995) Angiogenic potential of the avian somite. Dev Dyn 202(2):165–171PubMedCrossRefGoogle Scholar
  75. Wilting J, Schneider M, Papoutski M, Alitalo K, Christ B (2000) An avian model for studies of embryonic lymphangiogenesis. Lymphology 33(3):81–94PubMedGoogle Scholar
  76. Wilting J, Papoutsi M, Othman-Hassan K, Rodriguez-Niedenführ M, Pröls F, Tomarev SI, Eichmann A (2001) Development of the avian lymphatic system. Microsc Res Tech 55(2):81–91PubMedCrossRefGoogle Scholar
  77. Yusuf F, Brand-Saberi B (2006) The eventful somite: patterning, fate determination and cell division in the somite. Anat Embryol 211(Suppl 1):21–30PubMedGoogle Scholar
  78. Yusuf F, Brand-Saberi B (2012) Myogenesis and muscle regeneration. Histochem Cell Biol 138(2):187–199PubMedCrossRefGoogle Scholar
  79. Yusuf F, Rehimi R, Dai F, Brand-Saberi B (2005) Expression of chemokine receptor CXCR4 during chick embryo development. Anat Embryol 210(1):35–41PubMedCrossRefGoogle Scholar
  80. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393(6685):595–599PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Maryna Masyuk
    • 1
  • Aisha Abduelmula
    • 1
  • Gabriela Morosan-Puopolo
    • 1
  • Veysel Ödemis
    • 3
    • 4
  • Rizwan Rehimi
    • 1
  • Nargis Khalida
    • 1
  • Faisal Yusuf
    • 1
  • Jürgen Engele
    • 3
  • Hirokazu Tamamura
    • 5
  • Carsten Theiss
    • 1
    • 2
  • Beate Brand-Saberi
    • 1
    Email author
  1. 1.Medical Faculty, Department of Anatomy and Molecular EmbryologyRuhr-University BochumBochumGermany
  2. 2.Department of Cytology, Institute of AnatomyRuhr-University BochumBochumGermany
  3. 3.Medical Faculty, Institute of AnatomyUniversity of LeipzigLeipzigGermany
  4. 4.Faculty of Medicine and Health SciencesCarl von Ossietzky University OldenburgOldenburgGermany
  5. 5.Department of Medicinal Chemistry, Institute of Biomaterials and BioengineeringTokyo Medical and Dental UniversityTokyoJapan

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