Laminins in the developing and adult human small intestine: Relation with the functional absorptive unit

Developmental Dynamics

Volumn 236, Issue 7, 2007, Pages 1980-1990

  Teller, Inga C ^a   Auclair, Joëlle ^a   Herring, Elizabeth ^a   Gauthier, Rémy ^a   Ménard, Daniel ^a   Beaulieu, Jean François ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Basement membrane; Development; Epithelium; Human; Intestine; Laminins; Protein; Transcript

Indexed keywords

LAMININ;

ARTICLE; BASEMENT MEMBRANE; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; INTESTINE ABSORPTION; INTESTINE CRYPT; INTESTINE EPITHELIUM; INTESTINE VILLUS; MESENCHYME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMALL INTESTINE; TRANSCRIPTION REGULATION;

GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTESTINE, SMALL; LAMININ;

EID: 34447499028     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21186     Document Type: Article

References (76)

1. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC, Kleinman HK, Marinkovich MP, Martin GR, Mayer U, Meneguzzi G, Miner JH, Miyazaki K, Patarroyo M, Paulsson M, Quaranta V, Sanes JR, Sasaki T, Sekiguchi K, Sorokin LM, Talts JF, Tryggvason K, Uitto J, Virtanen I, von der Mark K, Wewer UM, Yamada Y, Yurchenco PD. 2005. A simplified laminin nomenclature. Matrix Biol 24:326-332.
2. Basora N, Vachon PH, Herring-Gillam FE, Perreault N, Beaulieu JF. 1997. Relation between integrin alpha7Bbeta1 expression in human intestinal cells and enterocytic differentiation. Gastroenterology 113:1510-1521.
3. Basora N, Desloges N, Chang Q, Bouatrouss Y, Gosselin J, Poisson J, Sheppard D, Beaulieu JF. 1998. Expression of the alpha9beta1 integrin in human colonic epithelial cells: resurgence of the fetal phenotype in a subset of colon cancers and adenocarcinoma cell lines. Int J Cancer 75:738-743.
4. Basora N, Herring-Gillam FE, Boudreau F, Perreault N, Pageot LP, Simoneau M, Bouatrouss Y, Beaulieu JF. 1999. Expression of functionally distinct variants of the beta(4)A integrin subunit in relation to the differentiation state in human intestinal cells. J Biol Chem 274:29819-29825.
5. Beaulieu JF. 1992. Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine. J Cell Sci 102:427-436.
6. Beaulieu JF. 1997. Extracellular matrix components and integrins in relationship to human intestinal epithelial cell differentiation. Prog Histochem Cytochem 31:1-78.
7. Beaulieu JF, Quaroni A. 1991. Clonal analysis of sucrase-isomaltase expression in the human colon adenocarcinoma Caco-2 cells. Biochem J 280:599-608.
8. Beaulieu JF, Vachon PH. 1994. Reciprocal expression of laminin A-chain isoforms along the crypt-villus axis in the human small intestine. Gastroenterology 106: 829-839.
9. Beaulieu JF, Vachon PH, Chartrand S. 1991. Immunolocalization of extracellular matrix components during organogenesis in the human small intestine. Anat Embryol (Berl) 183:363-369.
10. Belkin AM, Stepp MA. 2000. Integrins as receptors for laminins. Microsc Res Tech 51:280-301.
11. Boettner B, Van Aelst L. 2002. The RAS-putin effect. Genes Dev 16:2033-2038.
12. Bouatrouss Y, Herring-Gillam FE, Gosselin J, Poisson J, Beaulieu JF. 2000. Altered expression of laminins in Crohn's disease small intestinal mucosa. Am J Pathol 156:45-50.
13. Champliaud MF, Virtanen I, Tiger CF, Korhonen M, Burgeson R, Gullberg D. 2000. Posttranslational modifications and beta/gamma chain associations of human laminin alpha1 and laminin alpha5 chains: purification of laminin-3 from placenta. Exp Cell Res 259:326-335.
14. Colognato H, Yurchenco PD. 2000. Form and function: the laminin family of heterotrimers. Dev Dyn 218:213-234.
15. De Arcangelis A, Georges-Labouesse E. 2000. Integrin and ECM functions: roles in vertebrate development. Trends Genet 16:389-395.
16. De Arcangelis A, Neuville P, Boukamel R, Lefebvre O, Kedinger M, Simon-Assmann P. 1996. Inhibition of laminin alpha 1-chain expression leads to alteration of basement membrane assembly and cell differentiation. J Cell Biol 133: 417-430.
17. Doi M, Thyboll J, Kortesmaa J, Jansson K, Iivanainen A, Parvardeh M, Timpl R, Hedin U, Swedenborg J, Tryggvason K. 2002. Recombinant human laminin-10 (alpha5beta1gamma1). Production, purification, and migration-promoting activity on vascular endothelial cells. J Biol Chem 277:12741-12748.
18. Doliana R, Bellina I, Bucciotti F, Mongiat M, Perris R, Colombatti A. 1997. The human alpha3b is a "full-sized" laminin chain variant with a more widespread tissue expression than the truncated alpha3a. FEBS Lett 417:65-70.
19. Dufour G, Demers MJ, Gagne D, Dydensborg AB, Teller IC, Bouchard V, Degongre I, Beaulieu JF, Cheng JQ, Fujita N, Tsuruo T, Vallee K, Vachon PH. 2004. Human intestinal epithelial cell survival and anoikis. Differentiation state-distinct regulation and roles of protein kinase B/Akt isoforms. J Biol Chem 279: 44113-44122.
20. Dydensborg AB, Auclair J, Herring E, Teller IC, Menard D, Beaulieu JF. 2006a. Crypt-restricted expression of the integrin a6A subunit in the human intestinal epithelium: implication for proliferation but not differentiation. Gastroenterology 130:A-334.
21. Dydensborg AB, Herring E, Auclair J, Tremblay E, Beaulieu JF. 2006b. Normalizing genes for quantitative RT-PCR in differentiating human intestinal epithelial cells and adenocarcinomas of the colon. Am J Physiol Gastrointest Liver Physiol 290:G1067-G1074.
22. Ekblom P, Lonai P, Talts JF. 2003. Expression and biological role of laminin-1. Matrix Biol 22:35-47.
23. Engvall E, Earwicker D, Haaparanta T, Ruoslahti E, Sanes JR. 1990. Distribution and isolation of four laminin variants; tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul 1:731-740.
24. Escaffit F, Boudreau F, Beaulieu JF. 2005a. Differential expression of claudin-2 along the human intestine: Implication of GATA-4 in the maintenance of claudin-2 in differentiating cells. J Cell Physiol 203:15-26.
25. Escaffit F, Perreault N, Jean D, Francoeur C, Herring E, Rancourt C, Rivard N, Vachon PH, Pare F, Boucher MP, Auclair J, Beaulieu JF. 2005b. Repressed E-cadherin expression in the lower crypt of human small intestine: a cell marker of functional relevance. Exp Cell Res 302: 206-220.
26. Francoeur C, Escaffit F, Vachon PH, Beaulieu JF. 2004. Proinflammatory cytokines TNF-alpha and IFN-gamma alter laminin expression under an apoptosis-independent mechanism in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 287:G592-598.
27. Fujiwara H, Kikkawa Y, Sanzen N, Sekiguchi K. 2001. Purification and characterization of human laminin-8. Laminin-8 stimulates cell adhesion and migration through alpha3beta1 and alpha6beta1 integrins. J Biol Chem 276: 17550-17558.
28. Gustafsson E, Fassler R. 2000. Insights into extracellular matrix functions from mutant mouse models. Exp Cell Res 261: 52-68.
29. Hynes RO. 1996. Targeted mutations in cell adhesion genes: what have we learned from them? Dev Biol 180:402-412.
30. Ido H, Harada K, Yagi Y, Sekiguchi K. 2006. Probing the integrin-binding site within the globular domain of laminin-511 with the function-blocking monoclonal antibody 4C7. Matrix Biol 25:112-117.
31. Kadoya Y, Kadoya K, Durbeej M, Holmvall K, Sorokin L, Ekblom P. 1995. Antibodies against domain E3 of laminin-1 and integrin alpha 6 subunit perturb branching epithelial morphogenesis of submandibular gland, but by different modes. J Cell Biol 129:521-534.
32. Korhonen M, Virtanen I. 2001. Immunohistochemical localization of laminin and fibronectin isoforms in human placental villi. J Histochem Cytochem 49:313-322.
33. Lefebvre O, Sorokin L, Kedinger M, Simon-Assmann P. 1999. Developmental expression and cellular origin of the laminin alpha2, alpha4, and alpha5 chains in the intestine. Dev Biol 210:135-150.
34. Leivo I, Tani T, Laitinen L, Bruns R, Kivilaakso E, Lehto VP, Burgeson RE, Virtanen I. 1996. Anchoring complex components laminin-5 and type VII collagen in intestine: association with migrating and differentiating enterocytes. J Histochem Cytochem 44:1267-1277.
35. Li J, Tzu J, Chen Y, Zhang YP, Nguyen NT, Gao J, Bradley M, Keene DR, Oro AE, Miner JH, Marinkovich MP. 2003. Laminin-10 is crucial for hair morphogenesis. Embo J 22:2400-2410.
36. Lohi J, Oivula J, Kivilaakso E, Kiviluoto T, Frojdman K, Yamada Y, Burgeson RE, Leivo I, Virtanen I. 2000. Basement membrane laminin-5 is deposited in colorectal adenomas and carcinomas and serves as a ligand for alpha3beta1 integrin. Apmis 108:161-172.
37. Lotz MM, Nusrat A, Madara JL, Ezzell R, Wewer UM, Mercurio AM. 1997. Intestinal epithelial restitution. Involvement of specific laminin isoforms and integrin laminin receptors in wound closure of a transformed model epithelium. Am J Pathol 150:747-760.
38. Lussier C, Basora N, Bouatrouss Y, Beaulieu JF. 2000. Integrins as mediators of epithelial cell-matrix interactions in the human small intestinal mucosa. Microsc Res Tech 51:169-178.
39. Lussier C, Sodek J, Beaulieu JF. 2001. Expression of SPARC/osteonectm/ BM40 in the human gut: predominance in the stroma of the remodeling distal intestine. J Cell Biochem 81:463-476.
40. Menard D, Beaulieu JF. 1994. Human intestinal brush border membrane hydrolases. In: Bkaily G, editor. Membrane physiopathology. Norwell: Kluwer Academic Publisher. p 319-341.
41. Ménard D, Beaulieu J-F, Boudreau F, Perreault N, Rivard N, Vachon PH. 2006. Gastrointestinal tract. In: Unsicker K, Krieglstein K, editors. Cell signaling and growth factors in development: from molecules to organogenesis. Weinheim: Wiley-Vch. p 755-790.
42. Michele DE, Campbell KP. 2003. Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J Biol Chem 278:15457-15460.
43. Miner JH, Yurchenco PD. 2004. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20:255-284.
44. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR. 1997. The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel alphas isoform. J Cell Biol 137:685-701.
45. Nguyen NM, Senior RM. 2006. Laminin isoforms and lung development: all isoforms are not equal. Dev Biol 294:271-279.
46. Pageot LP, Perreault N, Basora N, Francoeur C, Magny P, Beaulieu JF. 2000. Human cell models to study small intestinal functions: recapitulation of the crypt-villus axis. Microsc Res Tech 49: 394-406.
47. Perreault N, Beaulieu JF. 1996. Use of the dissociating enzyme thermolysin to generate viable human normal intestinal epithelial cell cultures. Exp Cell Res 224: 354-364.
48. Perreault N, Vachon PH, Beaulieu JF. 1995. Appearance and distribution of laminin A chain isoforms and integrin alpha 2, alpha 3, alpha 6, beta 1, and beta 4 subunits in the developing human small intestinal mucosa. Anat Rec 242: 242-250.
49. Perreault N, Herring-Gillam FE, Desloges N, Belanger I, Pageot LP, Beaulieu JF. 1998. Epithelial vs mesenchymal contribution to the extracellular matrix in the human intestine. Biochem Biophys Res Commun 248:121-126.
50. Petajaniemi N, Korhonen M, Kortesmaa J, Tryggvason K, Sekiguchi K, Fujiwara H, Sorokin L, Thornell LE, Wondimu Z, Assefa D, Patarroyo M, Virtanen I. 2002. Localization of laminin alpha4-chain in developing and adult human tissues. J Histochem Cytochem 50:1113-1130.
51. Pouliot N, Connolly LM, Moritz RL, Simpson RJ, Burgess AW. 2000. Colon cancer cells adhesion and spreading on autocrine laminin-10 is mediated by multiple integrin receptors and modulated by EGF receptor stimulation. Exp Cell Res 261:360-371.
52. Pouliot N, Nice EC, Burgess AW. 2001. Laminin-10 mediates basal and EGF-stimulated motility of human colon carcinoma cells via alpha(3)beta(1) and alpha(6)beta(4) integrins. Exp Cell Res 266:1-10.
53. Rousselle P, Lunstrum GP, Keene DR, Burgeson RE. 1991. Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J Cell Biol 114:567-576.
54. Sasaki T, Fassler R, Hohenester E. 2004. Laminin: the crux of basement membrane assembly. J Cell Biol 164:959-963.
55. Simo P, Bouziges F, Lissitzky JC, Sorokin L, Kedinger M, Simon-Assmann P. 1992. Dual and asynchronous deposition of laminin chains at the epithelial-mesenchymal interface in the gut. Gastroenterology 102:1835-1845.
56. Simon-Assmann P, Bouziges F, Freund JN, Perrin-Schmitt F, Kedinger M. 1990. Type IV collagen mRNA accumulates in the mesenchymal compartment at early stages of murine developing intestine. J Cell Biol 110:849-857.
57. Simon-Assmann P, Duclos B, Orian-Rousseau V, Arnold C, Mathelin C, Engvall E, Kedinger M. 1994. Differential expression of laminin isoforms and alpha 6-beta 4 integrin subunits in the developing human and mouse intestine. Dev Dyn 201:71-85.
58. Simon-Assmann P, Lefebvre O, Bellissent-Waydelich A, Olsen J, Orian-Rousseau V, De Arcangelis A. 1998. The laminins: role in intestinal morphogenesis and differentiation. Ann N Y Acad Sci 859:46-64.
59. Simoneau A, Herring-Gillam FE, Vachon PH, Perreault N, Basora N, Bouatrouss Y, Pageot LP, Zhou J, Beaulieu JF. 1998. Identification, distribution, and tissular origin of the alpha5(IV) and alpha6(IV) collagen chains in the developing human intestine. Dev Dyn 212:437-447.
60. Teller IC, Beaulieu J-F. 2001. Interactions between laminin and epithelial cells in intestinal health and disease. Expert Reviews in Molecular Medicine 3:1-18 (http://www.ermm.cbcu.cam.ac.uk/01003623h.htm).
61. Tiger CF, Champliaud MF, Pedrosa-Domellof F, Thornell LE, Ekblom P, Gullberg D. 1997. Presence of laminin alpha5 chain and lack of laminin alphal chain during human muscle development and in muscular dystrophies. J Biol Chem 272:28590-28595.
62. Timpl R, Brown JC. 1996. Supramolecular assembly of basement membranes. Bioessays 18:123-132.
63. Tremblay E, Auclair J, Delvin E, Levy E, Menard D, Pshezhetsky AV, Rivard N, Seidman EG, Sinnett D, Vachon PH, Beaulieu JF. 2006. Gene expression profiles of normal proliferating and differentiating human intestinal epithelial cells: a comparison with the Caco-2 cell model. J Cell Biochem 99:1175-1186.
64. Turck N, Gross I, Gendry P, Stutzmann J, Freund JN, Kedinger M, Simon-Assmann P, Launay JF. 2005. Laminin isoforms: biological roles and effects on the intracellular distribution of nuclear proteins in intestinal epithelial cells. Exp Cell Res 303:494-503.
65. Vachon PH, Beaulieu JF. 1992. Transient mosaic patterns of morphological and functional differentiation in the Caco-2 cell line. Gastroenterology 103:414-423.
66. Vachon PH, Beaulieu JF. 1995. Extracellular heterotrimeric laminin promotes differentiation in human enterocytes. Am J Physiol 268:G857-867.
67. Vachon PH, Durand J, Beaulieu JF. 1993. Basement membrane formation and redistribution of the beta 1 integrins in a human intestinal co-culture system. Anat Rec 235:567-576.
68. Vainionpaa N, Kikkawa Y, Lounatmaa K, Miner JH, Rousselle P, Virtanen I. 2006. Laminin-10 and Lutheran blood group glycoproteins in adhesion of human endothelial cells. Am J Physiol Cell Physiol 290:C764-775.
69. Velling T, Tiger CF, Ekblom P, Gullberg D. 1999. Laminin alpha chains in colon carcinoma cell lines: detection of a truncated laminin alphal mRNA in Caco-2 cells. Exp Cell Res 248:627-633.
70. Virtanen I, Laitinen A, Tani T, Paakko P, Laitinen LA, Burgeson RE, Lehto VP. 1996. Differential expression of laminins and their integrin receptors in developing and adult human lung. Am J Respir Cell Mol Biol 15:184-196.
71. Virtanen I, Gullberg D, Rissanen J, Kivilaakso E, Kiviluoto T, Laitinen LA, Lehto VP, Ekblom P. 2000. Laminin alpha1-chain shows a restricted distribution in epithelial basement membranes of fetal and adult human tissues. Exp Cell Res 257:298-309.
72. Vuolteenaho R, Nissinen M, Sainio K, Byers M, Eddy R, Hirvonen H, Shows TB, Sariola H, Engvall E, Tryggvason K. 1994. Human laminin M chain (merosin): complete primary structure, chromosomal assignment, and expression of the M and A chain in human fetal tissues. J Cell Biol 124:381-394.
73. Weiser MM, Sykes DE, Killen PD. 1990. Rat intestinal basement membrane synthesis. Epithelial versus nonepithelial contributions. Lab Invest 62:325-330.
74. Wondimu Z, Gorfu G, Kawataki T, Smirnov S, Yurchenco P, Tryggvason K, Patarroyo M. 2006. Characterization of commercial laminin preparations from human placenta in comparison to recombinant laminins 2 (alpha2beta1gamma1), 8 (alpha4beta1-gamma1), 10 (alpha5beta1gamma1). Matrix Biol 25:89-93.
75. Yurchenco PD, Amenta PS, Patton BL. 2004. Basement membrane assembly, stability and activities observed through a developmentallens. Matrix Biol 22:521-538.
76. Zamurs L, Pouliot N, Gibson P, Hocking G, Nice E. 2003. Strategies for the purification of laminin-10 for studies on colon cancer metastasis. Biomed Chromatogr 17:201-211.