Structure and function of an early divergent form of laminin in hydra: A structurally conserved ECM component that is essential for epithelial morphogenesis

Development Genes and Evolution

Volumn 212, Issue 4, 2002, Pages 159-172

  Zhang, Xiaoming ^a,c,e   Fei, Kaiyin ^a,d   Agbas, Abdulbaki ^a,e   Yan, Li ^a,d   Zhang, Jinsong ^a   O'Reilly, Brooke ^a   Deutzmann, Rainer ^b   Sarras Jr , Michael ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c CHILDREN S MERCY HOSPITAL   (United States)

^d HARVARD UNIVERSITY   (United States)

^e UNIVERSITY OF KANSAS   (United States)

Author keywords

Extracellular matrix; Hydra; Integrin; Laminin; Morphogenesis

Indexed keywords

CELL SURFACE RECEPTOR; COMPLEMENTARY DNA; INTEGRIN; LAMININ; MESSENGER RNA; POLYPEPTIDE; PROTEIN SUBUNIT;

ALPHA CHAIN; AMINO ACID SEQUENCE; ANIMAL CELL; BETA CHAIN; BINDING AFFINITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL REGENERATION; COELENTERATE; CONTROLLED STUDY; DNA LIBRARY; ENDODERM; EPITHELIZATION; EXTRACELLULAR MATRIX; IN SITU HYBRIDIZATION; INVERTEBRATE; MOLECULAR CLONING; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, AFFINITY; CONSERVED SEQUENCE; ELECTROPORATION; EPITHELIUM; HYDRA; LAMININ; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; OLIGONUCLEOTIDES, ANTISENSE; ORGAN SPECIFICITY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

ANIMALIA; COELENTERATA; HYDRA; INVERTEBRATA; VERTEBRATA;

EID: 0036934521     PISSN: 0949944X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00427-002-0225-4     Document Type: Review

References (51)

1. Agbas A, Sarras MP Jr (1994) Evidence for cell surface extracellular matrix binding proteins in Hydra vulgaris. Cell Adhes Commun 2:59-73
2. Beck K, McCarthy RA, Chiqauet M, Masuda-Nakaguwa L, Schlage WK (1989) Structure of the basement membrane protein laminin: variations on a theme. In: Aebi U, Engel J (eds) Cytoskeletal and extracellular proteins: structure, interactions, and assembly. The 2nd EBSA Symposium. (Springer Series in Biophysics, vol 3) Springer, New York Berlin Heidelberg, pp 102-105
3. Benson S, Page L, Ingersoll E, Rosenthal E, Dungca K, Signor D (1999) Developmental characterization of the gene for laminin alpha-chain in sea urchin embryos. Mech Dev 81:1-2, 37-49
4. Bode HR, Dunne J, Heimfeld S, Huang L, Javois L, Koizumi O, Westerfield J, Yaross M (1986) Transdifferentiation occurs continuously in adult hydra. Curr Top Dev Biol 20:257-280
5. Burgeson RE, Chiquet M, Deutzmann R, Ekblom P, Engel J, Kleinman H, Martin G, Meneguzzi G, Paulsson M, Sanes J, Timpl R, Tryggvason K, Yamada Y, Yurchenco PD (1994) A new nomenclature for the laminins. Matrix Biol 14:209-221
6. Burke RD (1999) Invertebrate integrins: structure, function, and evolution. Int Rev Cytol 191:257-284
7. Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218:213-234
8. Deutzmann R, Fowler S, Zhang X, Boone K, Dexter S, Boot-Handford RP, Rachel R, Sarras MP (2000) Molecular, biochemical and functional analysis of a novel and developmentally important fibrillar collagen (Hcol-I) in hydra. Development 127(21):4669-4680
9. Engel J, Odermatt E, Engel A, Madri JA, Furthmayr H, Rohde H, Timpl R (1981) Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. J Mol Biol 150:97-120
10. Engvall E, Wewer UM (1996) Domains of laminin. J Cell Biochem 61:493-501
11. Flanagan WM, Kothavale A, Wagner RW (1996) Effects of oligonucleotide length, mismatches and mRNA levels on C-5 propyne-modified antisense potency. Nucleic Acids Res 24:2936-2941
12. Fowler SJ, Jose S, Zhang X, Deutzmann R, Sarras MP Jr, Boot-Handford RP (2000) Characterization of hydra type IV collagen. Type IV collagen is essential for head regeneration and its expression is up-regulated upon exposure to glucose. J Biol Chem 275(50):39589-39599
13. Garcia-Allonso L, Fetter RD, Goodman CS (1996) Genetic analysis of laminin A in Drosophila: extracellular matrix containing laminin A is required for ocellar axon pathfinding. Development 122:2611-2621
14. Garrsion K, MacKrell AJ, Fessler JH (1991) Drosophila laminin A chain sequence, interspecies comparison, and domain structure of a major carboxyl portion. J Biol Chem 266:22899-22904
15. Gierer A, Berking S, Bode HR, David CN, Flick KM, Hausmann G, Schaller H (1972) Regeneration of hydra from reaggregated cells. Nat New Biol 239:98-101
16. Gonzalez Agosti C, Stidwill R (1991) In vitro migration of Hydra nematocytes: the influence of the natural extracellular matrix (the mesoglea, of collagen type IV and type, laminin, and fibronectin) on cell attachment, migration parameters and patterns of cytoskeletal proteins. Cell Motil Cytoskeleton 20:215-227
17. Graner MW, Bunch TA, Baumgartner S, Kerschen A, Brower DL (1998) Splice variants of the Drosophila PS2 integrins differentially interact with RGD-containing fragments of the extracellular protein tiggrin, ten-m, and D laminin 2. J Biol Chem 273:18235-18241
18. Grens A, Mason E, Marsh JL, Bode HR (1995) Evolutionary conservation of a cell fate specification gene: the Hydra achaetescute homolog has proneural activity in Drosophila. Development 121(12):427-435
19. Grens A, Shimizu H, Hoffmeister SA, Bode HR, Fujisawa T (1999) The novel signal peptides, pedibin and Hym-346, lower positional value thereby enhancing foot formation in hydra. Development 126(3):517-524
20. Hawkins RL, Fan J, Hille MB (1995) Gastrulation in the sea urchin, Strongylocentrotus purpuratus, is disrupted by the small laminin peptides YIGSR and IKVAV. Cell Adhes Commun 3:167-177
21. Hopker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C (1999) Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401(6748):69-73
22. Hutter H, Vogel BE, Plenefisch JD, Norris CR, Proenca RB, Spieth J, Guo C, Mastwal S, Zhu X, Scheel J, Hedgecock EM (2000) Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287(5455):989-994
23. Lallier TE, Whittaker CA, DeSimone DW (1996) Integrin alpha 6 expression is required for early nervous system development in Xenopus laevis. Development 122:2539-2554
24. Leontovich AA, Zhang JS, Shimokawa K, Nagase H, Sarras MP Jr (2000) A novel hydra matrix metalloproteinase (HMMP) functions in extracellular matrix degradation, morphogepesis and the maintenance of differentiated cells in the foot process. Development 127(4):907-920
25. Martinez DE, Dirksen ML, Bode PM, Jamrich M, Steele RE, Bode HR (1997) Budhead, a fork head/HNF-3 homologue, is expressed during axis formation and head specification in hydra. Dev Biol 192(2):523-536
26. Minor JH, Li C (2000) Defective glomerulogenesis in the absence of laminin alpha 5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol 217:278-289
27. Montell DJ, Goodman CS (1988) Drosophila substrate adhesion molecule: sequence of laminin B1 chain reveals domains of homology with mouse. Cell 53:463-473
28. Patton BL, Miner JH, Chiu AY, Sanes JR (1997) Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J Cell Biol 139:1507-1521
29. Sambrook J, Fritsch EF, Maniatis T (1989) Construction and analysis of cDNA libraries. In: Ford N (ed) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. pp 8.64-8.51
30. Sarras MP Jr, Deutzmann R (2001) Hydra and Niccolo Paganini (1782-1840) - two peas in a pod? The molecular basis of extracellular matrix in the invertebrate, Hydra. Bioessays 23:716-724
31. Sarras MP Jr, Madden ME, Zhang X, Gunwar S, Huff JK, Hudson BG (1991a) Extracellular matrix (mesoglea) of Hydra vulgaris. I. Isolation and characterization. Dev Biol 148:481-494
32. Sarras MP Jr, Meador D, Zhang X (1991b) Extracellular matrix (mesoglea) of Hydra vulgaris. II. Influence of collagen and proteoglycan component on head regeneration. Dev Biol 148:495-500
33. Sarras MP Jr, Zhang X, Huff JK, St. John PL, Abrahamson DR (1993) Extracellular matrix (mesoglea) of Hydra vulgaris. III. Formation and function during morphogenesis of Hydra cell aggregates. Dev Biol 157:383-398
34. Sarras MP Jr, Yan L, Grens A, Zhang X, Agbas A, Huff JK, St. John PL, Abrahamson DR (1994) Cloning and biological function of laminin in Hydra vulgaris. Dev Biol 164(1):312-324
35. Schuger L, Skubitz AP, Zhang J, Sorokin L, He L (1997) Laminin alpha 1 chain synthesis in the mouse developing lung: requirement for epithelial-mesenchymal contact and possible role in bronchial smooth muscle development. J Cell Biol 139:553-562
36. Shimizu H, Zhang X, Zhang J, Leontovich A, Fei K, Yan L, Sarras MP Jr (2002) Epithelial morphogenesis in Hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development 129(6):1521-1532
37. Swofford DL (19 93) PAUP: phylogenetic analysis using parsimony. Illinois Natural History Survey, Champaign, III.
38. Tunggal P, Smyth N, Paulsson M, Ott M (2000) Laminins: structure and genetic regulation. Microsc Res Tech 51:214-227
39. Wagner RW (1994) Gene inhibition using antisense oligodeoxynucleotides. Nature 372:333-335
40. Wagner RW (1995) The state of the art in antisense research. Nat Med 1:1116-1118
41. 2+ current in cat atrial myocytes. J Physiol 526(Pt 1):57-68
42. Wessel GM, Marchase RB, McClay DR (1984) Ontogeny of the basal lamina in the sea urchin embryo. Dev Biol 103:235-245
43. r hydra metalloproteinase (HMP1), a member of the astacin family, localizes to the extracellular matrix of Hydra vulgaris in a head specific manner and has a developmental function. Development 121:1591-1602
44. Yan L, Leontovich A, Sarras MP Jr (2000a) Hydra metalloproteinase 1: a secreted astacin metalloproteinase whose apical axis expression is differentially regulated during head regeneration. Dev Biol 219:115-128
45. Yan L, Fei K, Zhang J, Dexter S, Sarras MP Jr (2000b) Identification and characterization of hydra metalloproteinase 2 (HMP2): a meprin-like astacin metalloproteinase that functions in foot morphogenesis. Development 127:128-141
46. Yoshida N, Ishii E, Nominzu M, Yamada Y, Mohri S, Kinukawa N, Matsuzaki A, Oshima K, Hara T, Miyazaki S (1999) The laminin-derived peptide YIGSR (Tyr-Ile-Gly-Ser-Arg) inhibits human pre-B leukaemic cell growth and dissemination to organs in SCID mice. Br J Cancer 80:1898-1904
47. Yoshida Y, Hosokawa K, Dantes A, Kotsuji F, Kleinman HK, Amsterdam A (2001) Role of laminin in ovarian cancer tumor growth and metastasis via regulation of Mdm2 and Bcl-2 expression. Int J Oncol 18:913-921
48. Zhang J, Leontovich A, Sarras MP Jr (2001) Molecular and functional evidence for early divergence of an endothelin-like system during metazoan evolution: analysis of the cnidarian, Hydra. Development 128:1607-1615
49. Zhang X, Sarras MP Jr (1994) Cell-extracellular matrix interactions under in vivo conditions during interstitial cell migration in Hydra vulgaris. Development 120(2):425-432
50. Zhang X, Hudson BG, Sarras MP Jr (1994) Hydra cell aggregate development is blocked by selective fragments of fibronectin and type IV collagen. Dev Biol 164(1):10-23
51. Ziegler U, Stidwill RP (1992) The attachment of nematocytes from the primitive invertebrate Hydra to fibronectin is specific and RGD-dependent. Exp Cell Res 202:281-286