Journal of Kerman University of Medical Sciences

Current Issue

By Issue

By Author

Author Index

Keyword Index

About Journal

Aims and Scope

JKMU Ethical Policies

Indexing and Abstracting

Related Links

FAQ

Peer Review Process

News

Metric

Editorial Policies

Data Sharing Policy

Developmental Changes of the Notochord and its Inductive Effects on the Adjacent Embryonic Germ Layers with Regard to the Role of Glycoconjugates

Document Type : Review Article

Author

Associate Professor of Anatomical Sciences, Department of Anatomy, Birjand University of Medical Sciences and Member of Cellular and Molecular Research Center, Birjand, Iran

Abstract

Notochord is an axial structure derived of embryonic mesoderm and in addition to structural supporting role in inducing nearby germinal layers, it has a basic role in formation of organs such as vertebral column, axial vessels, neural tube and primitive gut. This organ undergoes essential changes during the development process. First, arises from the primitive node and terms notochordal process, while containing a central canal. Then, transforms to notochordal plate and thereafter, changes to a cord called definitive notochord. Finally, it degenerates in centra and remains in intervertebral discs and makes its nucleus pulposus.
Glycoconjugates are macromolecules containing carbohydrates that interfere in some biological phenomena such as cell proliferation, differentiation, migration and apoptosis during the development of numerous organs. The terminal sugars of carbohydrate chains are mainly responsible for these duties.  These sugars are identifiable by using some polypeptides derived from plants and animals sources termed lectins. Lectins are linked exclusively to these sugars and the applied technique is called lectin histochemistry.
Investigation of the developmental changes of notochord using this technique has shown that different glycoconjugates with divers terminal sugars such as N-acetylgalactoseamine (GalNac), N-acetylclucoseamine (GlcNac), galactose (Gal), fucose (Fuc), mannose (Man) and neuraminic acid (NeuAc) and also Gal-GalNac and GalGlcNac disaccharides are expressed during morphogenesis period in this organ of different animal species.
Review of extensive studies carried out on development of notochord and its inductive role on nearby tissues has revealed that it is a highly glycosylated tissue and diverse glycoconjugates with different terminal sugars are expressed in it. Some of these molecules are probably involved in morphological changes of notochord while, the others are present in secreted substances from it and play key roles in its inductive effects on the nearby tissues.

Keywords

References
  1. Standring S (Editor in Chief). Gray's Anatomy: The anatomical basis of clinical practice, 39th ed, London, Elsevier Churchill Livingston, 2005; PP 194-6.
  2. Qasba PK. Involvement of sugars in protein–protein interactions. Carbohydrate Polymers 2000;41(3):293-309.
  3.      Zagris N. Extracellular matrix in development of the early embryo. Micron 2001;32(4):427-38.
  4. Götz W, Osmers R, Herken R. Localisation of extracellular matrix components in the embryonic human notochord and axial mesenchyme. J Anat 1995;186 (1): 111-21.
  5. Damjanov I. Biology of disease. Lectin cytochemistry and histochemistry. Lab Invest 1987;57:5-20.
  6. Zanetta JP, Kuchler S, Lehmann S, Badache A, Maschke S, Thomas D, et al. Glycoproteins and lectins in cell adhesion and cell recognition processes. Histochem J 1992;24(11):791-804.
  7. Spicer S, Schulte B. Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochem Cytochem 1992;40(1):1-38.
  8. Götz W, Quondamatteo F. Glycoconjugate distribution in early human notochord and axial mesenchyme. Acta histochem 2001;103(1):21-35.
  9. Quondamatteo F, Zieger J, Götz W, Miosge N, Herken R. Extensive glycosylation changes revealed by lectin histochemistry in morphologically normal prenatal tissues of the mouse mutant undulated (un/un). Anat Rec 2000; 258(3):243-51.
  10. Engel J. Laminins and other strange proteins. Biochemistry 1992; 31(44): 10643-51.
  11. Leivo I, Vaheri A, Timpl R, Wartiovaara J. Appearance and distribution of collagens and laminin in the early mouse embryo. Dev biol 1980;76(1):100-14.
  12. Haas TA, Plow EF. Integrin-ligand interactions: a year in review. Curr Opin Cell Biol 1994; 6(5): 656-62.
  13. Ruoslahti E, Öbrink B. Common principles in cell adhesion. Exp Cell Res 1996; 227 (1): 1-11.
  14. DeGrauw TJ, Liwnicz BH. Lectins are markers of neuronal migration and differentiation in rat brain. Dev Neurosci 1986; 8(4): 236-42.
  15. Wilson DB, Wyatt DP. Patterns of lectin binding during mammalian neurogenesis. J Anat 1995; 186(Pt 1): 209-16.
  16. Streit WJ, Schulte BA, Balentine DJ, Spicer SS. Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J Histochem Cytochem 1985; 33(10):1042-52.
  17. Ebrahimi V, Vojoudi E, Fazel A, Ebrahimzadeh A. Histochemical Lectin Study of Glycoconjugates Terminal Sugars during Retina Ganglionic Cell Differentiation in Rat Eye. Horizon of Medical Sciences 2014; 20(2): 101-7 [persian].
    1. Mencucci R, Marini M, Gheri G, Vichi D, Sarchielli E, Bonaccini L, et al. Lectin binding in normal, keratoconus and cross-linked human corneas. Acta Histochem 2011;113(3):308-16.
  18.      Talaei KT, Arab M, Fazel A, Jalali M. A study of glycoconjugates of cell surface and extra cellular matrix of developing rat spiral limbus. J Ahwaz Univ Med Sci 2002; 33: 33-9 [Persian].
  19. Hassanzadeh Taheri MM, Nikravesh MR, Djalali M, Fazel AR, Ebrahimzadeh A, Ebrahimzadeh AR. Distribution of specific glycoconjugates in early mouse embryonic notochord and paraxial mesenchyme. Iranian Biomed J 2005; 9(1): 21-6.
  20. Heidari Z, Fazel AR, Moiin AA. Histochemical study of developing cartilage of primordial vertebrae in rat embryo. Cell Journal (Yakhteh) 2002; 4(15): 127-31 [Persian].
  21. Hassanzadeh Taheri MM, Ebrahimzadeh Bideskan AR, Miri MR. Regulatory Changes of N-Acetylgalactosamine Terminal Sugar in Early Mouse Embryonic Paraxial Mesenchyme. Cell Journal (Yakhteh) 2012; 14(2): 130- 41.
  22. Valbuena G, Madrid JF, Hernández F, Sáez FJ. Identification of fucosylated glycoconjugates in Xenopus laevis testis by lectin histochemistry. Histochem Cell Biol 2010; 134(2): 215-25.
  23. Miyanaka H, Nakamura T, Nishi N. Tissue-specific expression of fucosylated glycosphingolipid species in rat prostate. Biosci Biotechnol Biochem 2010; 74(6): 1261-6.
  24.      Ebrahimzadeh Bideskan AR, Hassanzadeh Taheri MM, Nikravesh MR, Fazel AR. Lectin histochemical study of vasculogenesis during rat pituitary morphogenesis. Iran J Basic Med Sci 2011;14(1):35-41.
  25. Ahi M, Zamansoltani F, Hassanzadeh Taheri MM, Ebrahimzadeh Bideskan AR The role of GalNac terminal sugar on adrenal gland development. Adv Biol Res 2007; 1(1-2): 34-9.
  26. Pasdar FA, Khooei A, Fazel A, Mahmoudi M, Nikravesh MR, Delui MK. Diagnostic value of lectins in differentiation of molar placentas. Iran J Basic Med Sci 2012;15(6):1140.
  27. Kitamura N, Guo S, Sato T, Hiraizumi S, Taka J, Ikekita M, et al. Prognostic significance of reduced expression of β‐N‐acetylgalactosaminylated N‐linked oligosaccharides in human breast cancer. Int J Cancer 2003;105(4):533-41.
  28. Arab MR, Rojhan AR, Jahantigh M, Mohammadi M. Lectin Histochemical Study of GalNac and GlcNac Containing Glycoconjugates in Colon Adenocarcinoma. Anatomical Sciences 2013; 10 (4) :29-33
  29. Arab MR, Salari S, Karimi M, Mofidpour H. Lectin histochemical study of cell surface glycoconjugate in gastric carcinoma using helix pomatia agglutinin. Acta Med Iran 2010; 48(4): 209-13.
  30. Sobral APV, Rego MJ, Cavalacanti CL, Carvalho Jr LB, Beltrão EI. ConA and UEA-I lectin histochemistry of parotid gland mucoepidermoid carcinoma. J Oral Sci 2010;52(1):49-54.
  31. Sadler TW. Langman's medical embryology, 11th ed, Phyladelphia, Lippincott Williams & Wilkins, 2011: PP 55-6.
  32. Moore KL, Persaud TVN, Torchia MG. The developing human: clinically oriented embryology: 8th ed,  Elsevier Health Sciences; 2015: PP 249-55.
  33. Dockter JL. Sclerotome induction and differentiation. Curr Top Dev Biol 2000; 48: 77-118.
  34. Hassanzadeh Taheri MM, Nikravesh M, Jalali M, Fazel A. Lectin histochemistry study of distribution of glycoconjugates on the notochordal cells during early morphogenesis in mouse embryos. Journal of Urmia University of Medical Sciences 2003; 14 (3): 187-97 [Persian].
  35. Choi KS, Harfe BD. Hedgehog signaling is required for formation of the notochord sheath and patterning of nuclei pulposi within the intervertebral discs. Proc Notl Acad Sci USA 2011; 108 (23): 9484-9.
  36. Choi KS, Lee C, Harfe BD. Sonic hedgehog in the notochord is sufficient for patterning of the intervertebral discs. Mech Dev 2012; 129 (9-12): 255-62.
  37. Hunter CJ, Matyas JR, Duncan NA. The notochordal cell in the nucleus pulposus: a review in the context of tissue engineering. Tissue Eng 2003; 9(4): 667-77.
  38. Oettinger HF, Thal G, Sasse J, Holtzer H, Pacifici M. Immunological analysis of chick notochord and cartilage matrix development with antisera to cartilage matrix macromolecules. Dev Biol 1985; 109(1): 63-71.
  39. Hennigar RA, Schulte BA, Spicer SS. Histochemical detection of glycogen using Griffonia simplicifolia agglutinin II. Histochem J 1986; 18(11-12): 589-96.
  40. Griffith CM, Sanders EJ. Changes in glycoconjugate expression during early chick embryo development: A lectin‐binding study. Anat Rec 1991;231(2):238-50.
  41. Tremble P, Chiquet-Ehrismann R, Werb Z. The extracellular matrix ligands fibronectin and tenascin collaborate in regulating collagenase gene expression in fibroblasts. Mol Biol Cell 1994; 5(4): 439-53.
  42. Aguiar DJ, Johnson SL, Oegema TR. Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp Cell Res 1999;246(1):129-37.
  43. Hoedt-Schmidt S, McClure J, Jasani MK, Kalbhen D. Immunohistochemical localization of articular cartilage proteoglycan and link protein in situ using monoclonal antibodies and lectin-binding methods. Histochemistry 1993;99(5):391-403.
  44. Hemming FJ, Saxod R. Regulated expression of keratan sulphate and peanut agglutinin binding sites during organogenesis in the developing chick. Histochem Cell Biol 1998; 110(2): 189-200.
  45. .Hassanzadeh Taheri MM, Nikravesh MR, Jalali M, Fazel AR. The role glycoconjugates in development of floor plate during early morphogenesis in mouse embryo. J Kerman University of Medical Sciences 2004; 11(2): 85-93 [Persian].
  46. Placzek M, Dodd J, Jessell TM. Discussion point: The case for floor plate induction by the notochord. Curr Opin Neurobiol 2000; 10(1): 15-22.
  47. Placzek M, Tessier-Lavigne M, Yamada T, Jessell T, Dodd J. Mesodermal control of neural cell identity: floor plate induction by the notochord. Science 1990; 250(4983): 985-8.
  48. Krengel S, Götz W, Herken R. Expression pattern of type II collagen mRNA during early vertebral development in the human embryo. Anat Embryol 1996; 193(1): 43-51.
  49. Varki A. Sialic acids as ligands in recognition phenomena. FASEB J 1997; 11(4): 248-55.
  50. Odent S, Attié-Bitach T, Blayau M, Mathieu M, Augé J, Delezoïde A, et al. Expression of the Sonic hedgehog (SHH) gene during early human development and phenotypic expression of new mutations causing holoprosencephaly. Hum Mol Genet 1999; 8(9): 1683-9.
  51. Nikravesh MR, Jalali M, Fazel A. Developmental Changes of Glycoconjugates in Early Mouse Embryonic Neuroepitelium, Notochordal and Surronding Mesenchymal Interactions. Yakhteh J 2002; 4(15): 157-63 [Persian].
  52. Cleaver O, Krieg PA. Notochord patterning of the endoderm. Dev Biol 2001; 234(1): 1-12.
  53. Gleiberman AS, Fedtsova NG, Rosenfeld MG. Tissue interactions in the induction of anterior pituitary: role of the ventral diencephalon, mesenchyme, and notochord. Dev Biol 1999; 213(2): 340-53.
  54. Eyal-Giladi H. The notochord as inductor of the orohypophysis in urodeles (Pleurodeles waltii). Proc K Med Wet (Amsterdam) 1958; 61: 224-34.
  55. Cooke J. Dynamics of the control of body pattern in the development of Xenopus laevis III. Timing and pattern after uv irradiation of the egg and after excision of presumptive head endo—mesoderm. Journal of embryology and experimental morphology 1985; 88(1): 135-50.
  56. Jessell TM, Dodd J. Floor plate-derived signals and the control of neural cell pattern in vertebrates. Harvey lectures 1990;86:87-128
  57. Spörle R, Schughart K. Neural tube morphogenesis. Curr Opin Genet Dev 1997; 7(4): 507-12.
  58. Colamarino SA, Tessier-Lavigne M. The role of the floor plate in axon guidance. Ann Rev Neurosci 1995; 18(1): 497-529.
  59. Basler K, Edlund T, Jessell TM, Yamada T. Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGFβ family member. Cell 1993; 73(4): 687-702.
  60. Masuda T, Fukamauchi F, Takeda Y, Fujisawa H, Watanabe K, Okado N, et al. Developmental regulation of notochord-derived repulsion for dorsal root ganglion axons. Mol Cell Neurosci 2004; 25(2): 217-27.
  61. Charrier JB, Lapointe F, Le Douarin NM, Teillet MA. Dual origin of the floor plate in the avian embryo. Development 2002;129 (20): 4785- 96.
  62. Le Douarin NM, Teillet M, Catala M. Neurulation in amniote vertebrates: a novel view deduced from the use of quail-chick chimeras. Int J Dev Biol 1998; 42: 909-16.
  63. Nikravesh MR, Jalali M, Fazel AR. Unique carbohydrate appearance of the floor plate during early neurolation. Iranian Biomedical Journal 2003;7(3):133-7.
  64. Brand-Saberi B, Ebensperger C, Wilting J, Balling R, Christ B. The ventralizing effect of the notochord on somite differentiation in chick embryos. Anat Embryol 1993; 188(3): 239-45.
  65. Rahbari R, Mazani M, Gol MM, Sagha M. Sclrotomal differentiation of somatic cells co-cultured with chicken embryonic notochord. Journal of Cell & Tissue (JCT) 2014; 5(1): 71-77 [Persian].
  66. Goulding M, Lumsden A, Paquette AJ. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 1994; 120(4): 957-71.
  67. Correia KM, Conlon RA. Surface ectoderm is necessary for the morphogenesis of somites. Mech Dev 2000; 91(1): 19-30.
  68. Denetclaw WF, Berdougo E, Venters SJ, Ordahl CP. Morphogenetic cell movements in the middle region of the dermomyotome dorsomedial lip associated with patterning and growth of the primary epaxial myotome. Development 2001;128(10):1745-55.
  69. Halpern ME, Ho RK, Walker C, Kimmel CB. Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 1993; 75(1): 99-111.
  70. Fleming A, Keynes R, Tannahill D. A central role for the notochord in vertebral patterning. Development 2004; 131(4): 873-80.
  71. Fleming A, Keynes RJ, Tannahill D. The role of the notochord in vertebral column formation. J Anatomy 2001; 199(1&2): 177-80.
  72. Kimelman D, Griffin KJ. Vertebrate mesendoderm induction and patterning. Curr Opin Genet Dev 2000; 10(4): 350-6.
  73. Nikravesh M, Fazel A, Jalali M. From mesenchyme to cartilage: Lectin histochemical studies of ventro-medial mesenchyme to the developing neural tube during embryonic period. Iran J Basic Med Sci 2002; 5(2): 100-6 [Persian].
  74. Goldstein AM, Fishman MC. Notochord regulates cardiac lineage in zebrafish embryos. Dev Biol 1998; 201(2): 247-52.
  75. Danos MC, Yost HJ. Role of Notochord in Specification of Cardiac Left–Right Orientation in Zebrafish and Xenopus. Dev Biol 1996; 177(1): 96-103.
  76. Bisgrove BW, Essner JJ, Yost HJ. Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. Development 2000; 127(16): 3567-79.
  77. Melloy PG, Ewart JL, Cohen MF, Desmond ME, Kuehn MR, Lo CW. No turning, a mouse mutation causing left–right and axial patterning defects. Dev Biol 1998; 193(1): 77-89.
  78. Davidson BP, Kinder SJ, Steiner K, Schoenwolf GC, Tam PP. Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. Dev Biol 1999; 211(1): 11-26.
  79. Fouquet B, Weinstein BM, Serluca FC, Fishman MC. Vessel patterning in the embryo of the zebrafish: guidance by notochord. Dev Biol 1997; 183 (1): 37-48.
  80. Sumoy L, Keasey JB, Dittman TD, Kimelman D. A role for notochord in axial vascular development revealed by analysis of phenotype and the expression of VEGR-2 in zebrafish flh and ntl mutant embryos. Mech Dev 1997; 63 (1): 15- 27.
  81. Reese DE, Hall CE, Mikawa T. Negative regulation of midline vascular development by the notochord. Dev Cell 2004; 6(5): 699-708.
  82. Risau W, Lemmon V. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol 1988; 125(2): 441-50.
  83. Kim J, Kim P, Hui CC. The VACTERL association: lessons from the Sonic hedgehog pathway. Clin Genet 2001; 59(5): 306-15.
  84. Charrier J-B, Lapointe F, Le Douarin NM, Teillet M-A. Anti-apoptotic role of Sonic hedgehog protein at the early stages of nervous system organogenesis. Development 2001;128(20):4011-20.
  85. Concordet JP, Lewis KE, Moore JW, Goodrich LV, Johnson RL, Scott MP, et al. Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 1996;122(9):2835-46.
  86. Isaacs HV, Pownall ME, Slack JMW. eFGF is expressed in the dorsal midline of Xenopus laevis. Int J Dev Biol 1995; 39 (4): 575-9
  87. Risau W. Embryonic angiogenesis factors. Pharmacol Ther 1991; 51(3): 371-6.
  88. Roghani M, Moscatelli D. Basic fibroblast growth factor is internalized through both receptor-mediated and heparan sulfate-mediated mechanisms. J Biol Chem 1992; 267(31): 22156-62.
  89. Hasanzadeh-Tahery MM, Nikravesh M, Jalaly M, Fazel A. Distribution of some Glycoconjugates in Notochord and axial vessels during early morphogenesis in Balb/C mouse embryos. Journal of Gorgan University of Medical Sciences 2003; 5(1): 1-9 [Persian].
  90. Kim SK, Hebrok M, Melton DA. Notochord to endoderm signaling is required for pancreas development. Development 1997;124(21):4243-52.
  91. Dilorio PJ, Moss JB, Sbrogna JL, Karlstrom RO, Moss LG. Sonic hedgehog is required early in pancreatic islet development. Dev Biol 2002; 244(1): 75-84.
  92. Schwitzgebel VM. Programming of the pancreas. Mol Cell Endocrinol 2001; 185(1): 99-108.
  93. Hebrok M, Kim SK, Melton DA. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev 1998; 12(11): 1705-13.
  94. Mortella A, O’Donnella BAM, Gilesb BS, Banniganb J, Puri AP. Adriamycin induces notochord hypertrophy with conservation of sonic hedgehog expression in abnormal ectopic notochord in the adriamycin rat model. Journal of pediatric surgery 2004;39(6):859-63.
  95. Merei JM. Notochord-gut failure of detachment and intestinal atresia. Pediatr Surg Int 2004; 20(6): 439-43.
  96. Ghanbari A, Khazaei M, Hashemi-Tabar M, Rabzia A, Fathi F, Bayat PD. Sonic hedgehog inhibition induces mouse embryonic stem cells to differentiate toward definitive endoderm. Indian J Exp Biol 2013; 51(3):201-7.
  97. Gillick J, Mooney E, Giles S, Bannigan J, Puri P. Notochord anomalies in the adriamycin rat model: a morphologic and molecular basis for the VACTERL association. J Pediatric Surg 2003;38(3):469-73.
  98. Domeneghini C, Arrighi S, Radaelli G, Bosi G, Veggetti A. Histochemical analysis of glycoconjugate secretion in the alimentary canal of Anguilla anguilla L. Acta histochem 2005; 106(6): 477-87.

100. Zanuzzi CN, Barbeito CG, Ortíz ML, Lozza FA, Fontana PA, Portiansky EL, et al. Glycoconjugate histochemistry in the small and large intestine of normal and Solanum glaucophyllum-intoxicated rabbits. Res Vet Sci 2010;89(2):214-22.

101. Bryk SG, Gheri G. Lectin histochemistry of enterocytes sugar residues in the gut of the chick embryo and of the newborn. Ital J Anat Embryol 2002; 107(1): 37-49.

102. George S, Oh Y, Lindblom S, Vilain S, Rosa AJ, Francis DH, et al. Lectin binding profile of the small intestine of five-week-old pigs in response to the use of chlortetracycline as a growth promotant and under gnotobiotic conditions.  J Anim Sci 2007; 85(7): 1640-50.

103. Hassanzadeh-Taheri MM, Hassanpour-Fard M, Kazemi T, Fazel AR. Distribution of some Glycoconjugates in the Notochord and Developing Gut during Early Morphogenesis in Balb/c Mouse Embryos. Zahedan Journal of Research in Medical Sciences 2012;14(3):7-12.

104. Fazel AR, Schulte BA, Spicer SS. Glycoconjugate unique to migrating primordial germ cells differs with genera. Anat Rec 1990; 228(2): 177-84.

 

 

 

Journal of Kerman University of Medical Sciences
Volume 23, Issue 5 - Serial Number 5
September and October 2016
Pages 649-670
Files
Share
How to cite
Statistics